Intraparenchymal nerve growth factor improves behavioral deficits while minimizing the adverse effects of intracerebroventricular delivery

Neuroscience

Volumn 124, Issue 4, 2004, Pages 743-755

  Pizzo, D P ^a,b   Thal, L J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

Acetylcholine; ACh; AD; Alzheimer's disease; Analysis of variance; ANOVA; CBF; ChAT; Choline acetyltransferase; Cholinergic basal forebrain; CSF; Hyperalgesia; Intraparenchymal NGF; Nucleus basalis magnocellularis; Schwann cell; Water maze

Indexed keywords

CHOLINE ACETYLTRANSFERASE; CYTOCHROME C; IBOTENIC ACID; NERVE GROWTH FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BRAIN CORTEX; CERVICAL SPINAL CORD; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; DOSE RESPONSE; DRUG DELIVERY SYSTEM; ENZYME ACTIVITY; HYPERALGESIA; INTRAPARENCHYMAL DRUG DELIVERY; LATERAL BRAIN VENTRICLE; MEDULLA OBLONGATA; NONHUMAN; OLIVARY NUCLEUS; PRIORITY JOURNAL; RAT; SCHWANN CELL; SPATIAL MEMORY; WEIGHT GAIN; WEIGHT REDUCTION;

ANIMALS; AVOIDANCE LEARNING; BASAL NUCLEUS OF MEYNERT; BEHAVIOR, ANIMAL; CEREBRAL CORTEX; CHOLINE O-ACETYLTRANSFERASE; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROSHOCK; HYPERALGESIA; HYPERPLASIA; IBOTENIC ACID; INJECTIONS; INJECTIONS, INTRAVENTRICULAR; MALE; MAZE LEARNING; MEDULLA OBLONGATA; NERVE GROWTH FACTOR; RATS; RATS, INBRED F344; SCHWANN CELLS; SPINAL CORD; WEIGHT GAIN; WEIGHT LOSS;

EID: 1542380985     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2003.12.041     Document Type: Article

References (49)

1. Bartus R.T., Dean R.L. 3rd, Beer B., Lippa A.S. The cholinergic hypothesis of geriatric memory dysfunction. Science. 217:1982;408-414.
2. Chen K.S., Gage F.H. Somatic gene transfer of NGF to the aged brain behavioral and morphological amelioration. J Neurosci. 15:1995;2819-2825.
3. Collerton D. Cholinergic function and intellectual decline in Alzheimer's disease. Neuroscience. 19:1986;1-28.
4. Conner J.M., Darracq M.A., Roberts J., Tuszynski M.H. Nontropic actions of neurotrophins subcortical nerve growth factor gene delivery reverses age-related degeneration of primate cortical cholinergic innervation. Proc Natl Acad Sci USA. 98:2001;1941-1946.
5. Coyle J.T., Price D.L., DeLong M.R. Alzheimer's disease a disorder of cortical cholinergic innervation. Science. 219:1983;1184-1190.
6. Cummings J.L., Kaufer D. Neuropsychiatric aspects of Alzheimer's disease the cholinergic hypothesis revisited. Neurology. 47:1996;876-883.
7. Day-Lollini P.A., Stewart G.R., Taylor M.J., Johnson R.M., Chellman G.J. Hyperplastic changes within the leptomeninges of the rat and monkey in response to chronic intracerebroventricular infusion of nerve growth factor. Exp Neurol. 145:1997;24-37.
8. Dekker A.J., Connor D.J., Thal L.J. The role of cholinergic projections from the nucleus basalis in memory. Neurosci Biobehav Rev. 15:1991;299-317.
9. Dekker A.J., Gage F.H., Thal L.J. 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. 48:1992;111-119.
10. Dekker A.J., Thal L.J. Effect of delayed treatment with nerve growth factor on choline acetyltransferase activity in the cortex of rats with lesions of the nucleus basalis magnocellularis dose requirements. Brain Res. 584:1992;55-63.
11. Dekker A.J., Winkler J., Ray J., Thal L.J., Gage F.H. Grafting of nerve growth factor-producing fibroblasts reduces behavioral deficits in rats with lesions of the nucleus basalis magnocellularis. Neuroscience. 60:1994;299-309.
12. 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. Upregulation of choline acetyltransferase activity in hippocampus and frontal cortex of elderly subjects with mild cognitive impairment. Ann Neurol. 51:2002;145-155.
13. Dirig D.M., Salami A., Rathbun M.L., Ozaki G.T., Yaksh T.L. Characterization of variables defining hindpaw withdrawal latency evoked by radiant thermal stimuli. J Neurosci Methods. 76:1997;183-191.
14. Dougherty K.D., Turchin P.I., Walsh T.J. Septocingulate and septohippocampal cholinergic pathways involvement in working/episodic memory. Brain Res. 810:1998;59-71.
15. Dunnett S.B., Everitt B.J., Robbins T.W. The basal forebrain-cortical cholinergic system interpreting the functional consequences of excitotoxic lesions. Trends Neurosci. 14:1991;494-501.
16. Dyck P.J., Peroutka S., Rask C., Burton E., Baker M.K., Lehman K.A., Gillen D.A., Hokanson J.L., O'Brien P.C. Intradermal recombinant human nerve growth factor induces pressure allodynia and lowered heat-pain threshold in humans. Neurology. 48:1997;501-505.
17. Eriksdotter Jönhagen M., Nordberg A., Amberla K., Beackman L., Ebendal T., Meyerson B., Olson L., Seiger A., Shigeta M., Theodorsson E., Viitanen M., Winblad B., Wahlund L.O. Intracerebroventricular infusion of nerve growth factor in three patients with Alzheimer's disease. Dement Geriatr Cogn Disord. 9:1998;246-257.
18. Fonnum F. Radiochemical micro assays for the determination of choline acetyltransferase and acetylcholinesterase activities. Biochem J. 115:1969;465-472.
19. Frick K.M., Price D.L., Koliatsos V.E., Markowska A.L. The effects of nerve growth factor on spatial recent memory in aged rats persist after discontinuation of treatment. J Neurosci. 17:1997;2543-2550.
20. Fusco M., Oderfeld-Nowak B., Vantini G., Schiavo N., Gradkowska M., Zaremba M., Leon A. Nerve growth factor affects uninjured, adult rat septohippocampal cholinergic neurons. Neuroscience. 33:1989;47-52.
21. Gill S.S., Patel N.K., Hotton G.R., O'Sullivan K., McCarter R., Bunnage M., Brooks D.J., Svendsen C.N., Heywood P. Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat Med. 9:2003;589-595.
22. Inui A. Feeding and body-weight regulation by hypothalamic neuropeptides-mediation of the actions of leptin. Trends Neurosci. 22:1999;62-67.
23. Isaacson L.G., Crutcher K.A. The duration of sprouted cerebrovascular axons following intracranial infusion of nerve growth factor. Exp Neurol. 131:1995;174-179.
24. Isaacson L.G., Saffran B.N., Crutcher K.A. Nerve growth factor-induced sprouting of mature, uninjured sympathetic axons. J Comp Neurol. 326:1992;327-336.
25. Krewson C.E., Saltzman W.M. Transport and elimination of recombinant human NGF during long-term delivery to the brain. Brain Res. 727:1996;169-181.
26. Lapchak P.A., Araujo D.M. NGF suppression of weight gain in adult female rats correlates with decreased hypothalamic cholecystokinin levels. Brain Res. 655:1994;12-16.
27. Lapchak P.A., Hefti F. BDNF and NGF treatment in lesioned rats effects on cholinergic function and weight gain. Neuroreport. 3:1992;405-408.
28. Lawrence C.B., Turnbull A.V., Rothwell N.J. Hypothalamic control of feeding. Curr Opin Neurobiol. 9:1999;778-783.
29. Lowry O.H., Rosenberg N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem. 193:1951;265-275.
30. Mandel R.J., Gage F.H., Clevenger D.G., Spratt S.K., Snyder R.O., Leff S.E. Nerve growth factor expressed in the medial septum following in vivo gene delivery using a recombinant adeno-associated viral vector protects cholinergic neurons from fimbria-fornix lesion-induced degeneration. Exp Neurol. 155:1999;59-64.
31. Markowska A.L., Koliatsos V.E., Breckler S.J., Price D.L., Olton D.S. Human nerve growth factor improves spatial memory in aged but not in young rats. J Neurosci. 14:1994;4815-4824.
32. Markowska A.L., Price D., Koliatsos V.E. Selective effects of nerve growth factor on spatial recent memory as assessed by a delayed nonmatching-to-position task in the water maze. J Neurosci. 16:1996;3541-3548.
33. Martínez-Serrano A., Fischer W., Söderström S., Ebendal T., Björklund A. Long-term functional recovery from age-induced spatial memory impairments by nerve growth factor gene transfer to the rat basal forebrain. Proc Natl Acad Sci USA. 93:1996;6355-6360.
34. Nutt J.G., Burchiel K.J., Comella C.L., Jankovic J., Lang A.E., Laws E.R. Jr, Lozano A.M., Penn R.D., Simpson R.K. Jr, Stacy M., Wooten G.F. Randomized, double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD. Neurology. 60:2003;69-73.
35. Ohno M., Yamamoto T., Watanabe S. Blockade of hippocampal M1 muscarinic receptors impairs working memory performance of rats. Brain Res. 650:1994;260-266.
36. Paxinos G., Watson C. The rat brain in stereotaxic coordinates. 1998;Academic Press, San Diego.
37. Petty B.G., Cornblath D.R., Adornato B.T., Chaudhry V., Flexner C., Wachsman M., Sinicropi D., Burton L.E., Peroutka S.J. The effect of systemically administered recombinant human nerve growth factor in healthy human subjects. Ann Neurol. 36:1994;244-246.
38. Pizzo D.P., Thal L.J., Winkler J. Mnemonic deficits in animals depend upon the degree of cholinergic deficit and task complexity. Exp Neurol. 177:2002;292-305.
39. Pizzo D.P., Winkler J., Sidiqi I., Waite J.J., Thal L.J. Modulation of sensory inputs and ectopic presence of Schwann cells depend upon the route and duration of nerve growth factor administration. Exp Neurol. 178:2002;91-103.
40. Rosicka M., Krsek M., Jarkovska Z., Marek J., Schreiber V. Ghrelin a new endogenous growth hormone secretagogue. Physiol Res. 51:2002;435-441.
41. Tiraboschi P., Hansen L.A., Alford M., Masliah E., Thal L.J., Corey-Bloom J. The decline in synapses and cholinergic activity is asynchronous in Alzheimer's disease. Neurology. 55:2000;1278-1283.
42. Tuszynski M.H., Thal L., HS U., Pay M.M., Blesch A., Conner J., Vahlsing H.L. Nerve growth factor gene therapy for Alzheimer's disease. J Mol Neurosci. 19:2002;207.
43. Walsh T.J., Herzog C.D., Gandhi C., Stackman R.W., Wiley R.G. Injection of IgG 192-saporin into the medial septum produces cholinergic hypofunction and dose-dependent working memory deficits. Brain Res. 726:1996;69-79.
44. Williams L.R. Hypophagia is induced by intracerebroventricular administration of nerve growth factor. Exp Neurol. 113:1991;31-37.
45. Winkler J., Power A.E., Ramirez G.A., Thal L.J. Short-term and complete reversal of NGF effects in rats with lesions of the nucleus basalis magnocellularis. Brain Res. 788:1998;1-12.
46. Winkler J., Ramirez G.A., Kuhn H.G., Peterson D.A., Day-Lollini P.A., Stewart G.R., Tuszynski M.H., Gage F.H., Thal L.J. Reversible Schwann cell hyperplasia and sprouting of sensory and sympathetic neurites after intraventricular administration of nerve growth factor. Ann Neurol. 41:1997;82-93.
47. Winkler J., Ramirez G.A., Thal L.J., Waite J.J. Nerve growth factor (NGF) augments cortical and hippocampal cholinergic functioning after p75NGF receptor-mediated deafferentation but impairs inhibitory avoidance and induces fear-related behaviors. J Neurosci. 20:2000;834-844.
48. Winkler J., Thal L.J. Effects of nerve growth factor treatment on rats with lesions of the nucleus basalis magnocellularis produced by ibotenic acid, quisqualic acid, and AMPA. Exp Neurol. 136:1995;234-250.
49. Zou L., Yuan X., Long Y., Shine H.D., Yang K. Improvement of spatial learning and memory after adenovirus-mediated transfer of the nerve growth factor gene to aged rat brain. Hum Gene Ther. 13:2002;2173-2184.