Biological therapies for Alzheimer's disease: Focus on trophic factors

Critical Reviews in Neurobiology

Volumn 10, Issue 2, 1996, Pages 205-238

  Koliatsos, Vassilis E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cholinergic neurons; Clinical trials; Dementia; Memory; Nerve growth factor; Neurodegenerative

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEUROTROPIN; SOMATOMEDIN C;

ALZHEIMER DISEASE; CHOLINERGIC NERVE CELL; HUMAN; MEMORY; NERVE DEGENERATION; NERVE REGENERATION; NEUROTROPISM; NONHUMAN; RAT; REVIEW; WORKING MEMORY;

EID: 0030452221     PISSN: 08920915     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevNeurobiol.v10.i2.40     Document Type: Review

References (160)

1. Purves, D., Body and Brain, Harvard University Press, Cambridge, 1988.
2. Ramón y Cajal, S., Degeneration and Regeneration of the Nervous System, Oxford University Press, London, 1928.
3. Björklund, A., Nobin, A., and Stenevi, U., Regeneration of central serotonin neurons after axonal degeneration induced by 5,6-dihydroxytryptamine, Brain Res., 50, 214, 1973.
4. Markowska, A. L., Breckler, S. J., Price, D. L., and Koliatsos, V. E., Nerve growth factor (NGF) induced hypertrophy of basal forebrain cholinergic neurons ameliorates spatial memory impairment in aged rats, 1995; Presented at Third Suncoast Workshop on the Neurobiology of Aging, Amelia Island, Florida.
5. Scheff, S. W., Synaptic reorganization after injury: the hippocampus as a model system, in Seil, F. J., Ed., Neural Regeneration and Transplantation, Alan R. Liss, New York, 1988, 137.
6. Reynolds, B. A. and Weiss, S., Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system, Science, 255, 1707, 1992.
7. Reis, D. J., Ross, R. A., Gilad, G., and Joh, T. H., Reaction of central catecholaminergic neurons to injury: model systems for studying the neurobiology of central regeneration and sprouting, in Cotman, C. W., Ed., Neuronal Plasticity, Raven Press, New York, 1978, 197.
8. Nottebohm, F., Ed., Hope for a New Neurology, The New York Academy of Sciences, New York, 1985.
9. Loeb, G. E., Neural prosthetic interfaces with the nervous system, Trends Neurosci., 12, 195, 1989.
10. Baldessarini, R. J., Chemotherapy in Psychiatry, Principles and Practice, Harvard University Press, Cambridge, 1985.
11. Alzheimer, A., Uber eine eigenartige Erkrankung der Hirnrinde, Zentralbl. Nervenheilkunde Psychiatrie, 30, 177, 1907.
12. James, W., The Principles of Psychology, Dover Publications, Inc., New York, 1950.
13. McGeer, P. L., McGeer, E., Rogers, J., and Sibley, J., Anti-inflammatory drugs and Alzheimer disease, Lancet, 335, 1037, 1990.
14. Rogers, J., Cooper, N. R., Webster, S., Schultz, J., McGeer, P. L., Styren, S. D., Civin, W. H., Brachova, L., Bradt, B., Ward, P., and Lieberburg, I., Complement activation by β-amyloid in Alzheimer disease, Proc. Natl. Acad. Sci. U.S.A., 89, 10016, 1992.
15. Sukhov, R. R., Troncoso, J. C., Kawas, C., and Koliatsos, V. E., Patterns of neuronal DNA fragmentation detected by TUNEL in Alzheimer's disease, Soc. Neurosci. Abstr., 21, 1726, 1995.
16. Koliatsos, V. E., Applegate, M. D., Kitt, C. A., Walker, L. C., DeLong, M. R., and Price, D. L., Aberrant phosphorylation of neurofilaments accompanies transmitter-related changes in rat septal neurons following transection of the fimbria-fornix, Brain Res., 482, 205, 1989.
17. Growdon, J. H., Treatment of Alzheimer's disease? N. Engl. J. Med., 18, 1306, 1992.
18. Growdon, J. H., Biological therapies for Alzheimer's disease, in Whitehouse, P. J., Ed., Dementia, F. A. Davis, Philadelphia, 1993, 375.
19. Marin, D. B. and Davis, K. L., Experimental therapeutics, in Psychopharmacology: The Fourth Generation of Progress, Bloom, F. E. and Kupfer, D. J., Eds., Raven Press, Ltd., New York, 1995, 1417.
20. Atack, J. R., Cholinesterases in human degenerative diseases, in Cholinergic Basis for Alzheimer Therapy, Becker, R. and Giacobini, E., Eds., Birkhäuser, Boston, 1991, 31.
21. Giacobini, E., Linville, D., Messamore, E., and Ogane, N., Toward a third generation of cholinesterase inhibitors, in Cholinergic Basis for Alzheimer Therapy, Becker, R. and Giacobini, E., Eds., Birkhäuser, Boston, 1991, 477.
22. Nordberg, A., Lilja, A., Lundqvist, H., Hartvig, P., Amberla, K., Viitanen, M., Warpman, U., Johansson, M., Hellström-Lindahl, E., Bjurling, P., Fasth, K.-J., Långström, B., and Winblad, B., Tacrine restores cholinergic nicotinic receptors and glucose metabolism in Alzheimer patients as visualized by positron emission tomography, Neurobiol. Aging, 13, 747, 1992.
23. Davis, D. L., Thal, L. J., Gamzu, E., Davis, C. S., Woolson, R. F., Gracon, S. I., Drachman, D. A., Schneider, L. S., Whitehouse, P. J., Hoover, T. M., Morris, J. C., Kawas, C. H., Knopman, D. S., Earl, N. L., Kumar, V., Doody, R. S., and The Tacrine Collaborative Study Group, A double-blind, placebo-controlled multicenter study of Tacrine in patients with Alzheimer's disease, N. Engl. J. Med., 327, 1253, 1992.
24. Knapp, M. J., Pharma, D., Knopman, D. S., Solomon, P. R., Pendlebury, W. W., Davis, C. S., and Gracon, S. I., A 30-week randomized controlled trial of high-dose tacrine in patients with Alzheimer's disease, JAMA, 271, 985, 1994.
25. Kang, J., Lemaire, H.-G., Unterbeck, A., Salbaum, J. M., Masters, C. L., Grzeschik, K.-H., Multhaup, G., Beyreuther, K., and Müller-Hill, B., The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor, Nature, 325, 733, 1987.
26. Hilbich, C., Kisters-Woike, B., Reed, J., Masters, C. L., and Beyreuther, K., Aggregation and secondary structure of synthetic amyloid βA4 peptides of Alzheimer's disease, J. Mol. Biol., 218, 149, 1991.
27. Ehrmann, D., Prey, N., and Stoeter, P., Do old patients with Down's syndrome develop premature brain atrophy? J. Neural Transm., 1, 54, 1989.
28. Sisodia, S. S., Koo, E. H., Beyreuther, K., Unterbeck, A., and Price, D. L., Evidence that β-amyloid protein in Alzheimer's disease is not derived by normal processing, Science, 248, 492, 1990.
29. Goate, A., Chartier-Harlin, M.-C., Mullan, M., Brown, J., Crawford, F., Fidani, L., Giuffra, L., Haynes, A., Irving, N., James, L., Mant, R., Newton, P., Rooke, K., Roques, P., Talbot, C., Pericak-Vance, M., Roses, A., Williamson, R., Rossor, M., Owen, M., and Hardy, J., Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease, Nature, 349, 704, 1991.
30. Chartier-Harlin, M.-C., Crawford, F., Houlden, H., Warren, A., Hughes, D., Fidani, L., Goate, A., Rossor, M., Roques, P., Hardy, J., and Mullan, M., Early-onset Alzheimer's disease caused by mutations at codon 717 of the β-amyloid precursor protein gene, Nature, 353, 844, 1991.
31. Murrell, J., Farlow, M., Ghetti, B., and Benson, M. D., A mutation in the amyloid precursor protein associated with hereditary Alzheimer's disease, Science, 254, 97, 1991.
32. Karlinsky, H., Vaula, G., Haines, J. L., Ridgley, J., Bergeron, C., Mortilla, M., Tupler, R. G., Percy, M. E., Robitaille, Y., Noldy, N. E., Yip, T. C. K., Tanzi, R. E., Gusella, J. F., Becker, R., Berg, J. M., Crapper McLachlan, D. R., and St. George-Hyslop, P. H., Molecular and prospective phenotypic characterization of a pedigree with familiar Alzheimer's disease and a missense mutation in codon 717 of the β-amyloid precursor protein gene, Neurology, 42, 1445, 1992.
33. Whyte, S., Beyreuther, K., and Masters, C. L., Rational therapeutic strategies for Alzheimer's disease, in Neurodegenerative Diseases, Calne, D. B., Ed., W. B. Saunders, Philadelphia, 1994, 647.
34. Haass, C., Hung, A. Y., and Selkoe, D. J., Processing of β-amyloid precursor protein in microglia and astrocytes favors an internal localization over constitutive secretion, J. Neurosci., 11, 3783, 1991.
35. Chéramy, A., Romo, R., Godeheu, G., Baruch, P., and Glowinski, J., In vivo presynaptic control of dopamine release in the cat caudate nucleus - II. Facilitatory or inhibitory influence of L-glutamate, Neuroscience, 19, 1081, 1986.
36. McGeer, P. L., Akiyama, H., Itagaki, S., and McGeer, E. G., Activation of the classical complement pathway in brain tissue of Alzheimer patients, Neurosci. Lett., 107, 341, 1989.
37. Strittmatter, W. J., Saunders, A. M., Schmechel, D., Pericak-Vance, M., Enghild, J., Salvesen, G. S., and Roses, A. D., Apolipoprotein E: high-avidity binding to β-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease, Proc. Natl. Acad. Sci. U.S.A., 90, 1977, 1993.
38. Saunders, A. M., Strittmatter, W. J., Schmechel, D., St. George-Hyslop, P. H., Pericak-Vance, M. A., Joo, S. H., Rosi, B. L., Gusella, J. F., Crapper-MacLachlan, D. R., Alberts, M. J., Hulette, C., Crain, B., Goldgaber, D., and Roses, A. D., Association of apolipoprotein E allele ∈4 with late-onset familial and sporadic Alzheimer's disease, Neurology, 43, 1467, 1993.
39. Roses, A. D. and Saunders, A., Head injury, amyloid β and Alzheimer's disease, Nature Med., 1, 603, 1995.
40. Nicoll, J. A. R., Roberts, G. W., and Graham, D. I., Apolipoprotein E ∈ 4 allele is associated with deposition of amyloid β-protein following head injury, Nature Med., 1, 135, 1995.
41. Poirier, J., Apolipoprotein E in animal models of CNS injury and in Alzheimer's disease, Trends Neurosci., 17, 525, 1994.
42. Levy-Lahad, E., Wasco, W., Poorkaj, P., Romano, D. M., Oshima, J., Pettingell, W. H., Yu, C.-E., Jondro, P. D., Schmidt, S. D., Wang, K., Crowley, A. C., Fu, Y.-H., Guenette, S. Y., Galas, D., Nemens, E., Wijsman, E. M., Bird, T. D., Schellenberg, G. D., and Tanzi, R. E., Candidate gene for the chromosome 1 familial Alzheimer's disease locus, Science, 269, 973, 1995.
43. Sherrington, R., Rogaev, E. I., Liang, Y., Rogaeva, E. A., Levesque, G., Ikeda, M., Chi, H., Lin, C., Li, G., Holman, K., Tsuda, T., Mar, L., Foncin, J.-F., Bruni, A. C., Montesi, M. P., Sorbi, S., Rainero, I., Pinessi, L., Nee, L., Chumakov, I., Pollen, D., Brookes, A., Sanseau, P., Polinsky, R. J., Wasco, W., Da Silva, H. A. R., Haines, J. L., Pericak-Vance, M. A., Tanzi, R. E., Roses, A. D., Fraser, P. E., Rommens, J. M., and St. George-Hyslop, P. H., Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease, Nature, 375, 754, 1995.
44. Levi-Montalcini, R. and Booker, B., Destruction of the sympathetic ganglia in mammals by an antiserum to a nerve-growth protein, Proc. Natl. Acad. Sci. U.S.A., 46, 384, 1960.
45. Levi-Montalcini, R. and Hamburger, V., Selective growth stimulating effects of mouse sarcoma on the sensory and sympathetic nervous system of the chick embryo, J. Exp. Zool., 116, 321, 1951.
46. Goedert, M., Fine, A., Hunt, S. P., and Ullrich, A., Nerve growth factor mRNA in peripheral and central rat tissues and in the human central nervous system: lesion effects in the rat brain and levels in Alzheimer's disease, Mol. Brain Res., 1, 85, 1986.
47. Goedert, M., Fine, A., Dawbarn, D., Wilcock, G. K., and Chao, M. V., Nerve growth factor receptor mRNA distribution in human brain: normal levels in basal forebrain in Alzheimer's disease, Mol. Brain Res., 5, 1, 1989.
48. Koliatsos, V. E., Price, D. L., Clatterbuck, R. E., Markowska, A. L., Olton, D. S., and Wilcox, B. J., Neurotrophic strategies for treating Alzheimer's disease: lessons from basic neurobiology and animal models, Ann. N.Y. Acad. Sci., 695, 292, 1993.
49. Lauder, J. M. Neurotransmitters as growth regulatory signals: role of receptors and second messengers, Trends Neurosci., 16, 233, 1993.
50. Ruegg, M. A., Tsim, K. W. K., and Horton, S. E., The agrin gene codes for a family of basal lamina proteins that differ in function and distribution, Neuron, 8, 691, 1992.
51. Reist, N. E., Werle, M. J., and McMahan, U. J., Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions, Neuron, 8, 865, 1992.
52. Ferguson, I. A., Schweitzer, J. B., and Johnson, E. M., Jr., Basic fibroblast growth factor: receptor-mediated internalization, metabolism, and anterograde axonal transport in retinal ganglion cells, J. Neurosci., 10, 2176, 1990.
53. McDonald, N. Q., Lapatto, R., Murray-Rust, J., Gunning, J., Wlodawer, A., and Blundell, T. L., New protein fold revealed by a 2,3-Å resolution crystal structure of nerve growth factor, Nature, 354, 411, 1991.
54. Cohen, S., Purification and metabolic effects of a nerve growth-promoting protein from snake venom, J. Biol. Chem., 234, 1129, 1959.
55. Bocchini, V. and Angeletti, P. U., The nerve growth factor: purification as a 30,000-molecular-weight protein, Proc. Natl. Acad. Sci. U.S.A., 64, 787, 1969.
56. Angeletti, R. H. and Bradshaw, R. A., Nerve growth factor from mouse submaxillary gland: amino acid sequence, Proc. Natl. Acad. Sci. U.S.A., 68, 2417, 1971.
57. Barde, Y.-A., Edgar, D., and Thoenen, H., Purification of a new neurotrophic factor from mammalian brain, EMBO J., 1, 549, 1982.
58. Leibrock, J., Lottspeich, F., Hohn, A., Hofer, M., Hengerer, B., Masiakowski, P., Thoenen, H., and Barde, Y.-A., Molecular cloning and expression of brain-derived neurotrophic factor, Nature, 341, 149, 1989.
59. Hohn, A., Liebrock, J., Bailey, K., and Barde, Y.-A., Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family, Nature, 344, 339, 1990.
60. Rosenthal, A., Goeddel, D. V., Nguyen, T., Lewis, M., Shih, A., Laramee, G. R., Nikolics, K., and Winslow, J. W., Primary structure and biological activity of a novel human neurotrophic factor, Neuron, 4, 767, 1990.
61. Maisonpierre, P. C., Belluscio, L., Squinto, S., Ip, N. Y., Furth, M. E., Lindsay, R. M., and Yancopoulos, G. D., Neurotrophin-3: a neurotrophic factor related to NGF and BDNF, Science, 247, 1446, 1990.
62. Hilton, D. J., LIF: lots of interesting functions, Trends Biochem. Sci., 17, 72, 1992.
63. Lin, L.-F. H., Mismer, D., Lile, J. D., Armes, L. G., Butler, E. T. III, Vannice, J. L., and Collins, F., Purification, cloning, and expression of ciliary neurotrophic factor (CNTF), Science, 246, 1023, 1989.
64. Adler, R., Landa, K. B., Manthorpe, M., and Varon, S., Cholinergic neuronotrophic factors: intraocular distribution of trophic activity for ciliary neurons, Science, 204, 1434, 1979.
65. Stöckli, K. A., Lottspeich, F., Sendtner, M., Masiakowski, P., Carroll, P., Götz, R., Lindholm, D., and Thoenen, H., Molecular cloning, expression and regional distribution of rat ciliary neurotrophic factor, Nature, 342, 920, 1989.
66. Masu, Y., Wolf, E., Holtmann, B., Sendtner, M., Brem, G., and Thoenen, H., Distribution of the CNTF gene results in motor neuron degeneration, Nature, 365, 27, 1993.
67. Bazan, J. F., Neuropoietic cytokines in the hematopoietic fold, Neuron, 7, 197, 1991.
68. Hall, A. K. and Rao, M. S., Cytokines and neurokines: related ligands and related receptors, Trends Neurosci., 15, 35, 1992.
69. Ip, N. Y., Nye, S. H., Boulton, T. G., Davis, S., Taga, T., Li, Y., Birren, S. J., Yasukawa, K., Kishimoto, T., Anderson, D. J., Stahl, N., and Yancopoulos, G. D., CNTF and LIF act on neuronal cells via shared signaling pathways that involve the IL-6 signal transducing receptor component gp130, Cell, 69, 1121, 1992.
70. Henderson, J. T., Seniuk, N. A., Richardson, P. M., Gauldie, J., and Roder, J. C., Systemic administration of ciliary neurotrophic factor induces cachexia in rodents, J. Clin. Invest., 93, 2632, 1994.
71. Abraham, J. A., Whang, J. L., Tumolo, A., Mergia, A., Friedman, J., Gospodarowicz, D., and Fiddes, J. C., Human basic fibroblast growth factor: nucleotide sequence and genomic organization, EMBO J., 5, 2523, 1986.
72. Baird, A. and Böhlen, P., Fibroblast growth factors, in Peptide Growth Factors and Their Receptors I, Sporn, M. B. and Roberts, A. B., Eds., Springer-Verlag, New York, 1991.
73. Risau, W., Developing brain produces an angiogenesis factor, Proc. Natl. Acad. Sci. U.S.A., 83, 3855, 1986.
74. Yanagisawa-Miwa, A., Uchida, Y., Nakamura, F., Tomaru, T., Kido, H., Kamijo, T., Sugimoto, T., Kaji, K., Utsuyama, M., Kurashima, C., and Ito, H., Salvage of infarcted myocardium by angiogenic action of basic fibroblast growth factor, Science, 257, 1401, 1992.
75. Rechler, M. M. and Nissley, S. P., Insulin-like growth factors, in Peptide Growth Factors and Their Receptors I, Sporn, M. B. and Roberts, A. B., Eds., Springer-Verlag, New York, 1991, 263.
76. Guler, H.-P., Zapf, J., and Froesch, R., Short-term metabolic effects of recombinant human insulin-like growth factor I in healthy adults, N. Engl. J. Med., 317, 137, 1987.
77. Caroni, P. and Grandes, P., Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin-like growth factors, J. Cell Biol., 110, 1307, 1990.
78. Schaar, D. G., Sieber, B. A., Dreyfus, C. F., and Black, I. B., Regional and cell-specific expression of GDNF in rat brain, Exp. Neurol., 124, 368, 1993.
79. Cameron, V. A., Nishimura, E., Mathews, L. S., Lewis, K. A., Sawchenko, P. E., and Vale, W. W., Hybridization histochemical localization of activin receptor subtyped in rat brain, pituitary, ovary, and testis, Endocrinology, 134, 799, 1994.
80. Lin, L.-F. H., Doherty, D. H., Lile, J. D., Bektesh, S., and Collins, F., GDNF: A glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons, Science, 260, 1130, 1993.
81. Henderson, C. E., Phillips, H. S., Pollock, R. A., Davies, A. M., Lemeulle, C., Armanini, M., Simpson, L. C., Moffet, B., Vandlen, R. A., Koliatsos, V. E., and Rosenthal, A., GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle, Science, 266, 1062, 1994.
82. Oppenheim, R. W., Houenou, L. J., Johnson, J. E., Lin, L.-F. H., Li, L., Lo, A. C., Newsome, A. L., Prevette, D. M., and Wang, S., Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF, Nature, 373, 344, 1995.
83. Yan, Q., Matheson, C., and Lopez, O. T., In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons, Nature, 373, 341, 1995.
84. Beck, K. D., Valverde, J., Alexi, T., Poulsen, K., Moffat, B., Vandlen, R. A., Rosenthal, A., and Hefti, F., Mesencephalic dopaminergic neurons protected by GDNF from axotomy-induced degeneration in the adult brain, Nature, 373, 339, 1995.
85. Tomac, A., Lindqvist, E., Lin, L.-F. H., Ögren, S. O., Young, D., Hoffer, B. J., and Olson, L., Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo, Nature, 373, 335, 1995.
86. + toxicity, EMBO J., 14, 736, 1995.
87. Rodriguez-Tébar, A., Dechant, G., and Barde, Y.-A., Binding of brain-derived neurotrophic factor to the nerve growth factor receptor, Neuron, 4, 487, 1990.
88. Meakin, S. O. and Shooter, E. M., The nerve growth factor family of receptors, Trends Neurosci., 15, 323, 1992.
89. Rabizadeh, S., Oh, J., Zhong, L.-T., Yang, J., Bitler, C. M., Butcher, L. L., and Bredesen, D. E., Induction of apoptosis by the low-affinity NGF receptor, Science, 261, 345, 1993.
90. Dobrowsky, R. T., Werner, M. H., Castellino, A. M., Chao, M. V., and Hannun, Y. A., Activation of the sphingomyelin cycle through the low-affinity neurotrophin receptor, Science, 265, 1596, 1994.
91. Martin-Zanca, D., Oskam, R., Mitra, G., Copeland, T., and Barbacid, M., Molecular and biochemical characterization of the human trk proto-oncogene, Mol. Cell. Biol., 9, 24, 1989.
92. Chao, M. V., Neurotrophin receptors: a window into neuronal differentiation, Neuron, 9, 583, 1992.
93. Ehlers, M. D., Kaplan, D. R., Price, D. L., and Koliatsos, V. E., NGF-stimulated retrograde transport of trkA in the mammalian nervous system, J. Cell Biol., 130, 149, 1995.
94. Smeyne, R. J., Klein, R., Schnapp, A., Long, L. K., Bryant, S., Lewin, A., Lira, S. A., and Barbacid, M., Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene, Nature, 368, 246, 1994.
95. Crowley, C., Spencer, S. D., Nishimura, M. C., Chen, K. S., Pitts-Meek, S., Armanini, M. P., Ling, L. H., McMahon, S. B., Shelton, D. L., Levinson, A. D., and Phillips, H. S., Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons, Cell, 76, 1001, 1994.
96. Middlemas, D. S., Lindberg, R. A., and Hunter, T., trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors, Mol. Cell. Biol., 11, 143, 1991.
97. Klein, R., Smeyne, R. J., Wurst, W., Long, L. K., Auerbach, B. A., Joyner, A. L., and Barbacid, M., Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death, Cell, 75, 113, 1993.
98. Jones, K. R., Farinas, I., Backus, C., and Reichardt, L. F., Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development, Cell, 76, 989, 1994.
99. Ernfors, P., Lee, K. F., and Jaenisch, R., Mice lacking brain-derived neurotrophic factor develop with sensory deficits, Nature, 368, 147, 1994.
100. Ernfors, P., Lee, K.-F., Kucera, J., and Jaenisch, R., Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents, Cell, 77, 503, 1994.
101. Davis, S., Aldrich, T. H., Stahl, N., Pan, L., Taga, T., Kishimoto, T., Ip, N. Y., and Yancopoulos, G. D., LIFRβ and gp130 as heterodimerizing signal transducers of the tripartite CNTF receptor, Science, 260, 1805, 1993.
102. Davis, S., Aldrich, T. H., Valenzuela, D. M., Wong, V., Furth, M. E., Squinto, S. P., and Yancopoulos, G. D., The receptor for ciliary neurotrophic factor, Science, 253, 59, 1991.
103. Stahl, N., Boulton, T. G., Farruggella, T., Ip, N. Y., Davis, S., Witthuhn, B. A., Quelle, F. W., Silvennoinen, O., Barbieri, G., Pellegrini, S., Ihle, J. N., and Yancopoulos, G. D., Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-IL-6 β receptor components, Science, 263, 92, 1994.
104. DeChiara, T. M., Vejsada, R., Poueymirou, W. T., Acheson, A., Suri, C., Conover, J. C., Friedman, B., McClain, J., Pan, L., Stahl, N., Ip, N. Y., Kato, A., and Yancopoulos, G. D., Mice lacking the CNTF receptor, unlike mice lacking CNTF, exhibit profound motor neuron deficits at birth, Cell, 83, 313, 1995.
105. Kinney, H. C., Korein, J., Panigrahy, A., Dikkes, P., and Goode, R., Neuropathological findings in the brain of Karen Ann Quinlan. The role of the thalamus in the persistent vegetative state, N. Engl. J. Med., 330, 1469, 1994.
106. Wu, J.-Y., Cohen, L. B., and Falk, C. X., Neuronal activity during different behaviors in Aplysia: a distributed organization? Science, 263, 820, 1994.
107. Mishkin, M. and Appenzeller, T., The anatomy of memory. An inquiry into the roots of human amnesia has shown how deep structures in the brain may interact with perceptual pathways in outer brain layers to transform sensory stimuli into memories, Sci. Am., 256, 80, 1987.
108. Koliatsos, V. E., Price, W. L., Pardo, C. A., and Price, D. L., Ventral root avulsion: an experimental model of death of adult motor neurons, J. Comp. Neurol., 342, 35, 1994.
109. Hefti, F., Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections, J. Neurosci., 6, 2155, 1986.
110. Koliatsos, V. E., Applegate, M. D., Knüsel, B., Junard, E. O., Burton, L. E., Mobley, W. C., Hefti, F. F., and Price, D. L., Recombinant human nerve growth factor prevents retrograde degeneration of axotomized basal forebrain cholinergic neurons in the rat, Exp. Neurol., 112, 161, 1991.
111. Koliatsos, V. E., Nauta, H. J. W., Clatterbuck, R. E., Holtzman, D. M., Mobley, W. C., and Price, D. L., Mouse nerve growth factor prevents degeneration of axotomized basal forebrain cholinergic neurons in the monkey, J. Neurosci., 10, 3801, 1990.
112. Wilcox, B. J., Applegate, M. D., Portera-Cailliau, C., and Koliatsos, V. E., Nerve growth factor prevents apoptotic cell death in injured central cholinergic neurons, J. Comp. Neurol., 359, 573, 1995.
113. Koliatsos, V. E., Clatterbuck, R. E., Nauta, H. J. W., Knüsel, B., Burton, L. E., Hefti, F. F., Mobley, W. C., and Price, D. L., Human nerve growth factor prevents degeneration of basal forebrain cholinergic neurons in primates, Ann. Neurol., 30, 831, 1991.
114. Tuszynski, M. H., Sang, H., Yoshida, K., and Gage, F. H., Recombinant human nerve growth factor infusions prevent cholinergic neuronal degeneration in the adult primate brain, Ann. Neurol., 30, 625, 1991.
115. Koliatsos, V. E., Price, D. L., Gouras, G. K., Cayouette, M. H., Burton, L. E., and Winslow, J. W., Highly selective effects of nerve growth factor, brain-derived neurotrophic factor, and neurotrophin-3 on intact and injured basal forebrain magnocellular neurons, J. Comp. Neurol., 343, 247, 1994.
116. Peterson, D. A., Lucidi-Phillipi, C. A., Eagle, K. L., and Gage, F. H., Perforant path damage results in progressive neuronal death and somal atrophy in layer II of entorhinal cortex and functional impairment with increasing postdamage age, J. Neurosci., 14, 6872, 1994.
117. Capurso, S. A., Calhoun, M. E., Sukhov, R. R., Lukaczyk, T. A., Price, D. L., and Koliatsos, V. E., Apoptosis in the rat olfactory cortex after bulbectomy: an in vivo animal model of cortical cell death, Soc. Neurosci. Abstr., 21, 485, 1995.
118. Lindsay, R. M., Wiegand, S. J., Altar, C. A., and DiStefano, P. S., Neurotrophic factors: from molecule to man, Trends Neurosci., 17, 182, 1994.
119. Frick, K. M., Markowska, A. L., Price, D. L., Burton, L. E., Sukhov, R. R., and Koliatsos, V. E., Comparison of the effects of NGF and a recombinant pantrophin on spatial working memory in aged rats, Soc. Neurosci. Abstr., 21, 548, 1995.
120. Clatterbuck, R. E., Price, D. L., and Koliatsos, V. E., Ciliary neurotrophic factor prevents retrograde neuronal death in the adult central nervous system, Proc. Natl. Acad. Sci. U.S.A., 90, 2222, 1993.
121. Price, D. L., Koo, E. H., Wagster, M. V., Walker, L. C., Wenk, G. L., Applegate, M. D., Kitt, C. A., and Cork, L. C., Behavioral, cellular, and molecular biological studies of aged nonhuman primates, Adv. Neurol., 51, 83, 1990.
122. Fischer, W., Wictorin, K., Björklund, A., Williams, L. R., Varon, S., and Gage, F. H., Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor, Nature, 329, 65, 1987.
123. Markowska, A. L., Koliatsos, V. E., Breckler, S. J., Price, D. L., and Olton, D. S., Human nerve growth factor improves spatial memory in aged but not in young rats, J. Neurosci., 14, 4815, 1994.
124. Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., Caliendo, J., Hentati, A., Kwon, Y. W., Deng, H.-X., Chen, W., Zhai, P., Sufit, R. L., and Siddique, T., Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation, Science, 264, 1772, 1994.
125. Deng, H.-X., Hentati, A., Tainer, J. A., Iqbal, Z., Cayabyab, A., Hung, W.-Y., Getzoff, E. D., Hu, P., Herzfeldt, B., Roos, R. P., Warner, C., Deng, G., Soriano, E., Smyth, C., Parge, H. E., Ahmed, A., Roses, A. D., Hallewell, R. A., Pericak-Vance, M. A., and Siddique, T., Amyotrophic lateral sclerosis and structural defects in Cu, Zn superoxide dismutase, Science, 261, 1047, 1993.
126. Rosen, D. R., Siddique, T., Patterson, D., Figlewicz, D. A., Sapp, P., Hentati, A., Donaldson, D., Goto, J., O'Regan, J. P., Deng, H.-X., Rahmani, Z., Krizus, A., McKenna-Yasek, D., Cayabyab, A., Gaston, S. M., Berger, R., Tanzi, R. E., Halperin, J. J., Herzfeldt, B., Van den Bergh, R., Hung, W.-Y., Bird, T., Deng, G., Mulder, D. W., Smyth, C., Laing, N. G., Soriano, E., Pericak-Vance, M. A., Haines, J., Rouleau, G. A., Gusella, J. S., Horvitz, H. R., and Brown, R. H. Jr., Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis, Nature, 362, 59, 1993.
127. Price, D. L., Sisodia, S. S., Koliatsos, V. E., Borchelt, D. R., and Martin, L. J., Neuronal death: studies of amyotrophic lateral sclerosis, Alzheimer's disease, and their animal models, in Guide to Clinical Neurology, Mohr, J. P. and Gautier, J. C., Eds., Churchill Livingstone, New York, 1994.
128. Games, D., Adams, D., Alessandrini, R., Barbour, R., Berthelette, P., Blackwell, C., Carr, T., Clemens, J., Donaldson, T., Gillespie, F., Guido, T., Hagopian, S., Johnson-Wood, K., Khan, K., Lee, M., Leibowitz, P., Lieberburg, I., Little, S., Masliah, E., McConlogue, L., Montoya-Zavala, M., Mucke, L., Paganini, L., Penniman, E., Power, M., Schenk, D., Seubert, P., Snyder, B., Soriano, F., Tan, H., Vitale, J., Wadsworth, S., Wolozin, B., and Zhao, J., Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein, Nature, 373, 523, 1995.
129. Mocchetti, I., Theoretical basis for a pharmacology of nerve growth factor biosynthesis, Annu. Rev. Pharmacol. Toxicol., 32, 303, 1991.
130. Olsson, Y., Vascular permeability in the peripheral nervous system, in Peripheral Neuropathy, Dyck, P. J., Thomas, P. K., Lambert, E. H., and Bunge, R., Eds., W. B. Saunders, Philadelphia, 1984, 579.
131. Koliatsos, V. E. and Price, D. L., Nonhuman primate models in trophic factor research, in Animal Models of Neurological Disorders, Boulton, A. A., Baker, G. B., and Hefti, F., Humana Press, Clifton, NJ, 1993, 331.
132. Cayouette, M. H., Sukhov, R. R., Radeke, M. J., Price, D. L., and Koliatsos, V. E., Evidence for novel nerve growth factor (NGF)-responding neuronal populations in the mammalian brain, Soc. Neurosci. Abstr., 20, 1105, 1994.
133. Williams, L. R., Hypophagia is induced by intracerebroventricular administration of nerve growth factor, Exp. Neurol., 113, 31, 1991.
134. Isaacson, L. G., Saffran, B. N., and Crutcher, K. A., Intracerebral NGF infusion induces hyperinnervation of cerebral blood vessels, Neurobiol. Aging, 11, 51, 1990.
135. Olson, L., Nordberg, A., von Holst, H., Bäckman, L., Ebendal, T., Alafuzoff, I., Amberla, K., Hartvig, P., Herlitz, A., Lilja, A., Lundqvist, H., Långström, B., Meyerson, B., Persson, A., Viitanen, M., Winblad, B., and Seiger, Å., Nerve growth factor affects C-nicotine binding, blood flow, EEG, and verbal episodic memory in Alzheimer patient (case report), J. Neural Trans., 4, 79, 1992.
136. Glass, D. J. and Yancopoulos, G. D., The neurotrophins and their receptors, Trends Cell Biol., 3, 262, 1993.
137. Harbaugh, R. E., Intracerebroventricular bethanechol chloride administration in Alzheimer's disease, Ann. N.Y. Acad. Sci., 531, 174, 1988.
138. St. George-Hyslop, P., Crapper McLachlan, D., Tuda, T., Rogaev, E., Karlinsky, H., Lippa, C. F., and Pollen, D., Alzheimer's disease and possible gene interaction (letter to the Editor), Science, 263, 537, 1994.
139. Falsaperla, A., Monici Preti, P. A., and Oliani, C., Selegiline versus oxiracetam in patients with Alzheimer-type dementia, Clin. Ther., 12, 376, 1990.
140. Choi, D. W., Calcium: still center-stage in hypoxicishemic neuronal death, Trends Neurosci., 18, 58, 1995.
141. Sapolsky, R. M., Stress, the Aging Brain, and the Mechanisms of Neuron Death, MIT Press, Cambridge, 1992.
142. Coyle, J. T. and Puttfarcken, P., Oxidative stress, glutamate, and neurodegenerative disorders, Science, 262, 689, 1993.
143. Rothman, S. M. and Olney, J. W., Excitotoxicity and the NMDA receptor - still lethal after eight years, Trends Neurosci., 18, 57, 1995.
144. Bensimon, G., Lacomblez, L., Meininger, V., and The ALS/Riluzole Study Group, A controlled trial of riluzole in amyotrophic lateral sclerosis, N. Engl. J. Med., 330, 585, 1994.
145. Rowland, L. P., Riluzole for the treatment of amyotrophic lateral sclerosis - too soon to tell? N. Engl. J. Med., 330, 636, 1994.
146. Lipton, S. A. and Rosenberg, P. A., Excitatory amino acids as a final common pathway for neurologic disorders, N. Engl. J. Med., 330, 613, 1994.
147. Zhong, L.-T., Sarafian, T., Kane, D. J., Charles, A. C., Mah, S. P., Edwards, R. H., and Bredesen, D. E., bcl-2 inhibits death of central neural cells induced by multiple agents, Proc. Natl. Acad. Sci. U.S.A., 90, 4533, 1993.
148. Hengartner, M. O. and Horvitz, H. R., C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2, Cell, 76, 665, 1994.
149. Wilson, K. P., Black, J. -A. F., Thomson, J. A., Kim, E. E., Griffith, J. P., Navia, M. A., Murcko, M. A., Chambers, S. P., Aldape, R. A., Raybuck, S. A., and Livingston, D. J., Structure and mechanism of interleukin-1β converting enzyme, Nature, 370, 270, 1994.
150. Dubois-Dauphin, M., Frankowski, H., Tsujimoto, Y., Huarte, J., and Martinou, J.-C., Neonatal motoneurons overexpressing the bcl-2 protooncogene in transgenic mice are protected from axotomy-induced cell death, Proc. Natl. Acad. Sci. U.S.A., 91, 3309, 1994.
151. Gagliardini, V., Fernandez, P., Lee, R. K. K., Drexler, H. C. A., Rotello, R. J., Fishman, M. C., and Yuan, J., Prevention of vertebrate neuronal death by the crmA gene, Science, 263, 826, 1994.
152. Martinou, J.-C., Dubois-Dauphin, M., Staple, J. K., Rodriguez, I., Frankowski, H., Missotten, M., Albertini, P., Talabot, D., Catsicas, S., Pietra, C., and Huarte, J., Overexpression of bcl-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia, Neuron, 13, 1017, 1994.
153. Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A., Munday, N. A., Raju, S. M., Smulson, M. E., Yamin, T.-T., Yu, V. L., and Miller, D. K., Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis, Nature, 376, 37, 1995.
154. Schnabel, J., New Alzheimer's therapy suggested, Science, 260, 1719, 1993.
155. McGeer, P. L. and Rogers, J., Anti-inflammatory agents as a therapeutic approach to Alzheimer's disease, Neurology, 42, 447, 1992.
156. Rogers, J., Kirby, L. C., Hempelman, S. R., Berry, D. L., McGeer, P. L., Kasniak, A. W., Zalinski, J., Cofield, M., Mansukhani, L., Wilson, P., and Kogan, F., Clinical trial of indomethacin in Alzheimer's disease, Neurology, 43, 1609, 1993.
157. Friden, P. M., Walus, L. R., Watson, P., Doctrow, S. R., Kozarich, J. W., Bächman, C., Bergman, H., Hoffer, B., Bloom, F., and Granholm, A.-C., Blood-brain barrier penetration and in vivo activity of an NGF conjugate, Science, 259, 373, 1993.
158. Perry, R. H., Candy, J. M., Perry, E. K., Irving, D., Blessed, G., Fairbairn, A. F., and Tomlinson, B. E., Extensive loss of choline acetyltransferase activity is not reflected by neuronal loss in the nucleus of Meynert in Alzheimer's disease, Neurosci. Lett., 33, 311, 1982.
159. Levi-Montalcini, R., The nerve growth factor 35 years later, Science, 237, 1154, 1987.
160. Stahl, N., Farruggella, T. J., Boulton, T. G., Zhong, Z., Darnell, J. E. Jr., and Yancopoulos, G. D., Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors, Science, 267, 1349, 1995.