Physiology and pharmacology of natural and synthetic nonadenine-based purines in the nervous system

Drug Development Research

Volumn 45, Issue 3-4, 1998, Pages 356-372

  Rathbone, M P ^a   Middlemiss, P J ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2,6 DIAMINO N [[1 (1 OXOTRIDECYL) 2 PIPERIDYL]METHYL]HEXANAMIDE; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; ADENOSINE; ADENOSINE TRIPHOSPHATE; ADENOTIN; BINDING PROTEIN; DIZOCILPINE; GUANOSINE; GUANOSINE TRIPHOSPHATE; HYPOXANTHINE DERIVATIVE; LETEPRINIM; METHISOPRINOL; N METHYL DEXTRO ASPARTIC ACID; N(G) NITROARGININE METHYL ESTER; NERVE GROWTH FACTOR; PROTOPORPHYRIN TIN; PURINE; PURINE DERIVATIVE; SCOPOLAMINE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; CELL STRAIN; CONFERENCE PAPER; DRUG EFFECT; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NEUROPROTECTION; NEUROTROPISM; PATHOPHYSIOLOGY; PROTEIN INDUCTION; STRUCTURE ACTIVITY RELATION;

EID: 0032469376     PISSN: 02724391     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2299(199811/12)45:3/4<356::AID-DDR36>3.0.CO;2-C     Document Type: Conference Paper

References (108)

1. Abbracchio MP, Cattabeni E Clementi E Slier E. 1989. Adenosine receptors linked to adenylate cyclase activity in human neuroblastoma cells: Modulation during cell differentiation. Neuroscience 30:819-825.
2. Ang LC, Bhaumick B, Juurlink BHJ. 1993. Neurite promoting activity of insulin, insulin-like growth factor-I and nerve growth factor on spinal motoneurons is astrocyte dependent. Dev Brain Res 74:83-88.
3. Aurell A, Rosengren LE, Wikkelso C, Nordberg G, Haglid KG. 1989. The S-100 protein in cerebrospinal fluid: A simple ELISA method. J Neurol Sci 89:157-164.
4. Beal ME 1992. Mechanisms of excitotoxicity in neurologic diseases. FASEBJ 6:3338-3344.
5. Berger SJ, Carter JG, Lowry OH. 1985. Distribution of guanine deaminase in mouse brain. J Neurochem 44:1736-1740.
6. Brown ER, Gordon E 1970. Inosine-alkylamino alcohol complexes: Antiviral actions. Fed Proc 29:684."
7. Bruno V, Copani A, Battaglia G, Raffaele R, Shinozaki H, Nicoletti E 1994. Protective effect of the metabotropic glutamate receptor agonist, DCG-IV, against excilotoxic neuronal death. Eur J Pharmacol 256:109-112.
8. Bruno V, Sureda FX, Storto M, Casabona G, Caruso A, Knopfel T, Kühn R, Nicoletti E 1997. The neuroprotective activity of group-metabotropic glutamate receptors requires new protein synthesis and involves a glial-neuronal signaling. J Neurosci 17:1891-1897.
9. Bruno V, Battaglia G, Ngomba R, Nicoletti E 1998. A role for TGFß in vitro and in vivo neuroprotection mediated by glial metabotropic glutamate receptors. 6th Joint Meeting Italian, Hungarian and Polish Pharmacol Soc, Pisa (Italy) May 14-16 Abstract 5.
10. Buisson A, Choi DW. 1995. The inhibitor)' mGIuR agonist, S-4-carboxy3-hydroxy-phenyIglycine selectively attenuates NMDA neurotoxicity and oxygen-glucose deprivation-induced neuronal death. Neurophannacology 34:1081-1087.
11. Chiaia NL, Bennett Clarke CA, Crissman RS, Zheng L, Chen M, Rhoades RW. 1996. Effect of neonatal axoplasmic transport attenuation in the infraorbital nerve on vibrissae-related patterns in the rat's brainstem, thalamus and cortex. Eur J Neurosci 8:1601-1612.
12. Christjanson LJ, Middlemiss PJ, Rathbone ME 1993. Stimulation of astrocyte proliferation by purine and pyrimidine nucleotides and nucleosides. Glia 7:176-182.
13. Ciccarelli R, Sureda FX, Casabona G, Di lorio P, Caniso A, Spinella F, Condorelli DE Nicoletti E Caciagli E 1997. Opposite influence of the metabotropic glutamate receptor subtypes mGlu3 and -5 on astrocyte proliferation in culture. Glia 21:390-398.
14. 1 and group metabotropic glutamate receptors. Drug Dev Res 43:51.
15. Conner JM, Fass-Holmes B, Varon S. 1994. Changes in nerve growth factor immunoreactivity following entorhinal cortex lesions: Possible molecular mechanism regulating cholinergic sprouting. J Comp Neurol 345:409-418.
16. Davis RE Miller S, Herrnstadt C, Ghosh SS, Fahy E, Shinobu LA, Galasko D, Thai LJ, Beal M, Howell N, Parker WDJ. 1997. Mutations in mitochondrial cytochrome c oxidase genes segregate with late-onset Alzheimer disease. Proc Nail Acad Sci USA 94:4526-4531.
17. De Boni U, McLachlan DRC. 1985. Controlled production of paired helical filaments of the Alzheimer type in cultured human neurons by glutamate and aspartate. J Neurol Sci 68:105-118
18. Delafuente JC, Panush RS. 1988. Pharmacologie enhancement in the elderly: In vitro effects of isoprinosine. Clin Immunol Immunop 47:363-367.
19. Dessi F, Colle MA, Hauw JJ, Duyckaerts C. 1997. Accumulation of SNAP-25 immunoreactive material in axons of Alzheimer's disease. NeuroReport 8:3685-3659.
20. Diamond J, Holmes M, Coughlin M. 1992. Endogenous NGF and nerve impulses regulate the collateral sprouting of sensor)' avons in the skin of the adult rat. J Neurosci 12:1454-1466.
21. Diamond J, Pertens E, Holmes M, Urschel B, Pal R. 1996. Functionally adaptive changes are induced by collateral sprouting of nociceplive nerves, but not by NGF-induced hyperalgesia. Soc Neurosci Abst:711.5.
22. Di Giulio AM, Lesma E, Gorio A. 1995. Diabetic neuropathy in the rat. 1. Alcar augments the reduced levels and axoplasmic transport of substance E J Neurosci Res 40:414-419.
23. Di lorio P, Giuliani P, Ciccarelli R, Ballerini P, Battaglia G, Nicoletti F, Caciagli E1995. Effect of DCG-IV-sensitive metabotropic glutamate receptors on purine and glutamate release from rat hippocampal slices and cultured astrocytes. Res Commun Mol Pathol Pharmacol 87:57-58.
24. Di lorio P, Battaglia G, Ciccarelli R, Ballerini E Giuliani E Poli A, Nicolelti F Caciagli E 1996. Interaction between Al adenosine and class metabotropic receptors in the regulation of purine and glutamate release from rat hippocampal slices. J Neurochem 67:302-309.
25. DobleA. 1995. Excitatory amino acid receptors and neurodegeneration. Thérapie 50:319-337.
26. Doty B, Gordon E 1970. Inosin-alkylamino alcohol complexes: Enhancement of conditioned avoidance learning in rats. Fed Proc 29:684.
27. Durant RH, Dyken PR. 1983. The influence of inosiplex treatment on the neurological disability of patients with subacute sclerosing panencephalitis. Neurology 33:1053-1055.
28. Ethier MF, Dobson JG 1997. Adenosine stimulation of DNA synthesis in human endothelial cells. Am J Physiol 272:H1470-1479.
29. Fagan AM, Suhr ST, Lucidi-Phillipi CA, Peterson DA, Holtzman DA, Gage FH. 1997. Endogenous FGF-2 is important for cholinergic sprouting in the denervated hippocampus. J Neurosci 17:2499-2511.
30. Fanö G, Gysbers GW, Guamieri S, Pietrangelo T, Rathbone ME 1996. Extracellular GTP enhances NGF induced neunte outgrowth via increases in intracellular Ca2+. Drug Dev Res 37:168.
31. Farced GC, Tyler HR. 1971. The use of isoprinosine in patients with amyotrophic lateral sclerosis. Neurology121:937-940.
32. Fass B, Ramirez JJ. 1984. Effects of ganglioside treatments on lesioninduced behavioral impairments and sprouting in the CNS. J Neurosci Res. 12:445-158.
33. Fein T, Schulze E, Bär J, Schwabe U. 1994. Purification and characterization of an adenotin-like adenosine binding protein from human platelets. Naunyn Schmiedebergs Arch Pharmacol 349:374-380.
34. Fernandez HL, Hodges Savola C. 1994. Axoplasmic transport of calcitonin gene-related peptide in rat peripheral nerve as a function of age. Neurochem Res 19:1369-1377.
35. Freund HJ, Säbel BA, Witte OW. 1997. Brain plasticity. In: Advances in neurology, vol 73. Philadelphia: Lippincott-Raven.
36. Glasky AJ, Gordon J. 1986. Inosiplex treatment of acquired immunodeficiencies: A clinical model for effective immunomodulation. Meth Find Exp Clin Pharmacol 8:35-40.
37. Glasky AJ, Pfadenhauer EH, Settineri R, Ginsberg T. 1975. Isoprinosine, a purine derivative; metabolic, immunological and antiviral effects. In: Mewvissen H, editor. Combined immunodeficiency disease and adenosine deaminase deficiency, a molecular defect. San Francisco: Academic Press, p 157-171.
38. Glasky AJ, Melchior CL, Pirzadeh B, Heydari N, Ritzmann RE 1994. Effect of AIT-082, a purine analog, on working memory in normal and aged mice. Pliarmacol Biochem Behav 47:325-329.
39. Glasky AJ, Ritzmann RE Rathbone MR Middlemiss PJ, Crocker C. 1996. Neurolrophins, growth factors and mimetic agents as neuroprotectors in the treatment of Alzlieimer's disease. In: Becker R, Giacobini E, editors. Molecular biology to therapy. Boston: Birkhäuser. p 119-124.
40. Gu JG, Foga IO, Parkinson FE, Geiger CD. 1995. Involvement of bidirectional adenosine transporters in the release of L-[3H]adenosine from rat brain synaptosomal preparations. J Neurochem 64:21052110.
41. Gysbers JW, Rathbone ME 1992. Guanosine enhances NGF-stimulated neunte outgrowth in PC12 cells. NeuroReport 3:997-1000.
42. Gysbers JW, Rathbone MP 1996a. GTP and guanosine synergistically enhance NGF-induced neurite outgrowth from PC12 cells. Int J Dev Neurosci 14:19-34.
43. Gysbers JW, Rathbone MR 1998b. Neurite outgrowth in PC12 cells is enhanced by guanosine through both cAMP-dependent and -independent mechanisms. Neurosci Lett 220:175-178.
44. Gysbers JW, Middlemiss PJ, Rathbone ME 1994. Extracellular guanosine and GTP stimulate NGF and FGF-2 synthesis by mouse astrocyles. Soc Neurosci 24th Annual Meeting, Miami, FL, Nov 13-18. 20:13-14 Abstract 541.7.
45. Haun SE, Segeleon JE, Trapp VL, Clotz MA, Horrocks LA. 1996. Inosine mediates the protective effect of adenosine in rat astrocyte cultures subjected to combined glucose-oxygen deprivation. J Neurochem 67:2051-2059.
46. Heckers S, Ohtake T, Wiley RG, Lappi DA, Geula C, Mesulam MM. 1994. Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J Neurosci 14:1271-1289.
47. Herman MAR, Huang R, Hertz L, Rathbone ME 1993. Purine nucleoside uptake by mouse brain astrocytes. Soc Neurosci 23rd Annual Meeting, Washington, DC, Nov 7-12. 19:59 Abstract 33.2.
48. Herrero I, Castro E, Miras-Portugal MT, Sanchez-Prieto J. 1996. Two components of glutamate exocytosis differentially affected by presynaptic modulation. J Neurochem 67:2346-2354.
49. Hindley S, Rathbone MR 1994. Nitric oxide and carbon monoxide enhance neurite outgrowth from PC12 cells by activating soluble guanylate cyclase. IUPHAR Satellite Meeting "Nitric Oxide in the Nervous System-Neuropharmacology II" Laurentian Mountains, Quebec, Canada, July 22-24, p 140 Abstract 10.
50. Jan JE, Tingle AJ, Donald G, Kettyls M, Buckler WStJ, Dolman CL. 1979. Progressive rubella encephalitis: Clinical course and response to 'Isoprinosine.' Dev Med Child Neurol 21:648-652.
51. Juurlink BHJ, Walz W. 1998. Neural cell culture techniques. In: Boulton AA, Baker GB, Bateson AN, editors. In vitro neurochemical techniques, Neuromethods, vol 34. Totowa, NJ: Humana Press, pp 53-102.
52. Kim J-K, Rathbone MR Middlemiss P, Hughes DW, Smith R. 1991. Purinergic stimulation of astroblast proliferation: Guanosine and its nucleotides stimulate cell division in chick astroblasts. J Neurosci Res 28:442-445.
53. Laurenssen CM, Middlemiss PJ, Rathbone ME 1991. The role of purine nucleosides in the response of brain and other tissues to injury. I. Mechanisms of action of guanosine, adenosine metabolites and deoxynucleosides and nucleotides. 10th Annual Marcus Singer Symp Regeneration and Limb Develop, Indiana Univ. School of Med, Indianapolis, p 10 Abstract 8.
54. Laviada ID, Baudet C, Galve-Ropher I, Naveilhan E Brachet E 1995. Phosphatidylcholine-phospholipase C mediates the induction of nerve growth factor in cultured glial cells. FEES Lett 364:301-304.
55. Lee NH, Weinstock KG, Kirkness EC Earle-Hughes JA, Fuldner RA, Mannaros S, Glodek A, Gocayne JD, Adams MD, Kerlavage AR, Fraser CM, Venter CM. 1995. Comparative expressed-sequencetag analysis of differential gene expression profiles in PC-12 cells before and after nerve growth factor treatment. Proc Natl Acad Sci USA 92:8303-8307.
56. Lemmens R, Vanduffel L, Teuchy H, Culic 0.1996. Regulation of proliferation of LLC-MK2 cells by nucleosides and nucleotides: The role of ecto-enzymes. Biochem J 316:551-557.
57. Levi-Montalcini R, Skaper SD, Dal Toso R, Petrelli L, Leon A. 1996. Nerve growth factor: From neurotrophin to neurokine. Trends Neurosci 19:514-520.
58. Lewin GR, Ritter AM, Mendell LM. 1993. Nerve growth factor-induced hyperalgesia in the neonatal and adult rat. J Neurosci 13:21362148.
59. Liberski PE 1996. How do neurons degenerate in transmissible spongiform encephalopathies? Mol Chem Neuropathol 28:245-249.
60. Liberski PP, Budka II, Yanagihara R, Gajdusek DC. 1995. Neuroaxonal dystrophy in experimental Creutzfeldt-Jakob disease: Electron microscopical and immunohistochemical demonstration of neurofilament accumulations within affected neuntes. J Comp Pathol 112:243-255.
61. Lloyd GH, Fredholm BB. 1995. Involvement of adenosine deaminase and adenosine kinase in regulating extracellular adenosine concentration in rat hippocampal slices. Neurochem Int 26:387-395.
62. Loesche J, Steward 0.1977. Behavioral correlates of denervation and reinnervation of the hippocampal formation of the rat: Recover)' of alternation performance following unilateral entorhinal cortex lesions. Brain Res Bull 2:31-39.
63. LoPachin RM Jr, Lehning EJ. 1994. Acrylamide-induced distal axon degeneration: A proposed mechanism of action. Neurotoxicology 15:247-259.
64. Lorenzen A, Engelhardt J, Kerst B, Schwabe U. 1998. Heterogenous forms of adenotin-1 of different subcellular localization. Biochem Pharmacol 55:455-464.
65. Lynch G, Matthews DA, Mosko S, Parks T, Cotman C. 1972. Induced acetylcholinesterase-rich layer in rat dentate gyrus following entorhinal lesions. Brain Res 42:311-318.
66. Maragos WE Greenamyre JT, Penney JBJ, Young AB. 1987. Glutamate dysfunction in Alzheimer's disease: An hypothesis. Trends Neurosci 10:65-68.
67. March J, Field Shanley J, Turner WJ. 1973. Biochemical observations during a trial of inosiplex in senile dementia. J Am Geriatr Soc 21, : 372-378.
68. Mark RJ, Lovell MA, Markesbery WR, Uchida K, Mattson ME 1997. A role for 4-hydroxynonenal, an aldehydic product of lipid I peroxidation, in dismption of ion homeostasis and neuronal death induced by amyloid b-peptide. J Neurochem 68:255-264.
69. Mattson ME 1990. Antigenic changes similar to those seen in neurofibrillary tangles are elicited by glutamate and Ca2+ influx in cultured hippocampal neurons. Neuron 2:105-117.
70. Mattson ME Cheng B, Davis D, Bryant K, Lieberbtirg I, Rydel RE. 1992. Beta-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitoxicity. J Neurosci 12:37&-389.
71. Mattson MP, Rydel RE, Lieberburg I, Smith Swintosky VL. 1993. Altered calcium signaling and neuronal injury: Stroke and Alzheimer's disease as examples. Ann NY Acad Sci 679:1-21.
72. Mattson MP, Mark RJ, Furukawa K, Bruce AJ. 1997. Disruption of brain cell ion homeostasis in Alzheimer's disease by oxy radicals, and signalling pathways that protect therefrom. Chern Res Toxicol 10:507-517.
73. McGeer PL, Eccles Sir JC, McGeer EG. 1987. Molecular neurobiology of the mammalian brain. New York: Plenum Press.
74. Mearow KM, Kril Y, Diamond J. 1993. Increased NGF mRNA expression in denervated rat skin. NeuroReport 4:351-354.
75. Medori R, Autilio-Gambetti L, Monaco S, Gambetti R 1985. Experimental diabetic neuropathy: Impairment of slow transport with changes in axon cross-sectional area. Proc Natl Acad Sci USA 82:7716-7720.
76. Meghji P, Tuttle JB, Rubio R. 1989. Adenosine formation and release by embryonic chick neurons and glia in cell culture. J Neurochem 53:1852-1860.
77. 2y receptors. 13th Annual Meeting of Canadian College of Neuropsychophannacology (CCNP), Banff, Alberta, p 23 Abstract 7.
78. Middlemiss PJ, Glasky AJ, Rathbone MP, Werstuik E, Hindley S, Gysbers J. 1995. AIT-082, a unique purine derivative, enhances nerve growth factor mediated neurite outgrowth from PC 12 cells. Neurosci Lett 199:131-134.
79. 2+ release. Trends Pharmacol Sci 16:356-359.
80. Morley P, Hogan MJ, Hakim AM. 1994. Calcium-mediated mechanisms of ischémie injury and protection. Brain Pathol 4:37-47.
81. NaumannT, Deller T, Bender R, FrotscherM. 1997.192 IgG-saporinindrrced loss of cholinergic neurons in the septum abolishes cholinergic sprouting after unilateral entorhinal lesion in the rat. Eur J Neurosci 9:1304-1313.
82. Neary JT, Rathbone MP, Cattabeni F, Abbracchio MP, Burnstock G. 1996. Trophic actions of extracellular nucleolides and nucleosides on glial and neuronal cells. Trends Neurosci 19:13-18.
83. Nicoletti F, Bruno V, Copani A, Casabona G, Knöpfel T. 1996. Metabotropic glutamate receptors: A new target for the therapy of neurodegenerative disorders? Trends Neurosci 19:267-271.
84. Ordy JM, Thomas GJ, Volpe BT, Dunlap WP, Colombo PM. 1988. An animal model of human-type memory loss based on aging, lesion, forebrain ischemia and drug studies with the rat. Neurobiol Aging 9:667-683.
85. Paxinos G, Watson C. 1986. The rat brain irr stereotaxic coordinates. New York: Academic Press.
86. Phillis JW, Srnith-Barbour M, O'Regan MH. 1996. Changes in extracellular amino acid neurotransnritters and purines during and following ischemias of different durations in rat cerebral cortex. Neurochem Int 29:115-120.
87. Poli A, Contestabile A, Migani P, Rossi L, Rondelli C, Virgili M, Bissoli R, Bamabei 0.1985. Kainic acid differentially affects the synaptosomal release of endogenous ad exogenous amino acid neurotransnritters. J Neurochem 45:1677-1686.
88. Ranrirez JJ, McQuilkin M, Carrigan T, MacDonald K, Kelley MS. 1996. Progressive entorhinal cortex lesions accelerate hippocampal sprout-ing and spare spatial memory in rats. Proc Natl Acad Sci USA 93:15512-15517.
89. Rancurel G, Buge A. 1981. Herpetic necrosing encephalitis: Diagnosis and treatment with isoprinosine and interferon. Bull Mem Soc Med Paris 184:49-56.
90. Rathbone MR Juurlink B. 1993. Hippocampal neurons in vitro respond to extracellular gnanosine and GTP with neurite outgrowth and branching. Soc Neurosci 23rd Annual Meeting, Washington, DC, Nov 7-12, 19:38 Abstract 4.7.
91. Rathbone MP, Middlemiss PJ, Hooftman E, Kirn J-K. 1990. Purinergic stimulation of astrocyte proliferation by picomolar concentrations of adenine and guanine nucleosides and nucleotides. 13th Annual Meeting of Canadian College of Neuropsychopharmacology (CCNP), Banff, Alberta, p. 22, Abstract 6.
92. Rathbone MP, Middlemiss PJ, Kirn J-K, Gysbers JW, DeForge SP, Smith RW, Hughes DW. 1992a. Adenosine and its nucleotides stimulate proliferation of chick astrocytes and human astrocytome cells. Neurosci Res 13:1-17.
93. Rathbone MR Christjanson L, DeForge S, DeLuca B, Gysbers JW, Hindley S, Jovetich M, Middlemiss PJ,Takhal S. 1992b. Extracellular purine nucleosides stimulate cell division and pathological and physiological implications. Med Hypoth 37:232-240.
94. Rathbone MP, DeForge S, DeLuca B, Gabel B, Laurenssen C, Middlemiss PJ. Parkinson S. 1992c. Purinergic stimulation of cell division and differentiation: Mechanisms and pharmacological implications. Med Hypoth 37:213-219.
95. Rathbone MR Middlemiss PJ, Andrew C, Caciagli F, Ciccarelli R, Di lorio P, Huang R. 1998. The trophic effects of purines and purinergic signaling in pathologic reactions of astrocytes. Alz Dis Assoc Dis 12:S3G-S45.
96. 2+ homeostasis, cell death, proliferation and differentiation. Chem Biol Interact 77:1-23.
97. Ritzmann RF, Kling A, Melchior CL, Glasky AJ. 1993. Effect of age and strain on working memory' in mice as measured by win-shift paradigm. Pharmacol Biochem Beliav 44:S05-S07.
98. Rudolpne KA, Schubert E 1997. Modulation of neuronal and glial cell function by adenosine and neuroprotection in vascular dementia. Beliav Brain Res 83:123-128.
99. Schubert R OgataT, Marchini C, Ferroni S, Rudolphi KA. 1997. Protective mechanisms of adenosine in neurons and glial cells. Ann NY Acad Sci 825:1-10.
100. Schwartz JP, Pearson J, Johnson EM. 1982. Effects of exposure to antiNGF on sensory neurons of adult rats and guinea pigs. Brain Res 244:378-381.
101. Seeburg PH. 1993. The molecular biology of the mammalian glutamate receptor channels. Trends Pharmacol Sci 14:297-303.
102. Selkoe DJ. 1997. Alzheimer's disease: Genotypes, phenotype, and treatments. Science 275:630-631.
103. Simon LN, Glasky AJ, Luebben G. 1968. Ribaminol enhancement of brain protein synthesis. Life Sci 7:15-21.
104. Strauss I, Williamson JM, Bertram EH, Lothman EW, Femandez EJ. 1997. Histological and lll magnetic resonance spectroscopic imaging analysis of quinolinic acid-induced damage to the rat striatum. Magnet Reson Med 37:24-33.
105. Sze CI, Troncoso JC, Kawas C, Mouton E Price DL, Martin LJ. 1997. Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease. J Neuropathol Exp Neur 56:933-944.
106. Tsang KY, Fudenberg HH, Gnacy MJ. 1983. Restoration of immune responses of aging hamsters by treatment with isoprinosine. J Clin Invest 71:1750-1755.
107. Tymianski M, Tator CH. 1996. Normal and abnormal calcium homeostasis in neurons: A basis for the pathophysiology of traumatic and ischémie central nervous system injury. Neurosurgery 38:1176-1195.
108. Uemura Y, Miller JM, Maison WR, Beal ME 1991. Neurochemical analysis of focal ischemia in rats. Stroke 22:1548-1553.