Neuropeptide alterations in the hippocampal formation and cortex of transgenic mice overexpressing β-amyloid precursor protein (APP) with the Swedish double mutation (APP23)

Neurobiology of Disease

Volumn 14, Issue 3, 2003, Pages 579-594

  Diez, Margarita ^a   Danner, Simone ^b   Frey, Peter ^b   Sommer, Bernd ^b   Staufenbiel, Matthias ^b   Wiederhold, Karl Heinz ^b   Hökfelt, Tomas ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

Aging; Amyloid; Lesion; Nerve injury; Neurodegeneration; Plaque; Transgene

Indexed keywords

ACETYLCHOLINESTERASE; AMYLOID PRECURSOR PROTEIN; AMYLOID PRECURSOR PROTEIN 23; CHOLECYSTOKININ; DYNORPHIN; ENKEPHALIN; GALANIN; MUTANT PROTEIN; NEUROPEPTIDE; NEUROPEPTIDE Y; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DYSTROPHY; ENZYME ASSAY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MOSSY FIBER; MOUSE; NEOCORTEX; NEUROPATHY; NONHUMAN; NORADRENERGIC NERVE; PEPTIDE ANALYSIS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SENILE PLAQUE; TRANSGENIC MOUSE; VASCULAR AMYLOIDOSIS; WILD TYPE;

EID: 0346218251     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2003.08.003     Document Type: Article

References (97)

1. Adams J.C. Biotin amplification of biotin and horseradish peroxidase signals in histochemical stains. J. Histochem. Cytochem. 40:1992;1457-1463.
2. Amstrong D.M., Terry R.D. Substance P immunoreactivity within neuritic plaques. Neurosci. Lett. 58:1985;139-144.
3. Amstrong D.M., Benzing W.C., Evans J., Terry R.D., Shields D., Hansen L.A. Substance P and somatostatin coexist within neuritic plaques implications for the pathogenesis of Alzheimer's disease . Neuroscience. 31:1989;663-671.
4. Arai H., Takahashi T., Kimura M., Noguchi I., Minami M., Iizuka R. Post mortem human brain tissue investigations of neurotransmitters in aging and in AD/SDAT. Racagni G., Brunelo N., Fukada T. Biological Psychiatry. 1991;131-133 Excerpta Medica, Amsterdam.
5. Bennett G.J., Xie Y.-K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain. 33:1988;87-107.
6. Boncristiano S., Calhoun M.E., Kelly P.H., Pfeifer M., Bondolfi L., Stalder M., Phinney A.L., Abramowski D., Sturchler-Pierrat C., Enz A., Sommer B., Staufenbiel M., Jucker M. Cholinergic changes in the APP23 transgenic mouse model of cerebral amyloidosis. J. Neurosci. 22:2002;3234-3243.
7. Bondolfi L., Calhoun M., Ermini F., Kuhn H.G., Wiederhold K.H., Walker L., Staufenbiel M., Jucker M. Amyloid-associated neuron loss and gliogenesis in the neocortex of amyloid precursor protein transgenic mice. J. Neurosci. 22:2002;515-522.
8. Bornemann K.D., Staufenbiel M. Transgenic mouse models of Alzheimer's disease. Ann. N. Y. Acad. Sci. 908:2000;260-266.
9. Bornemann K.D., Wiederhold K.H., Pauli C., Ermini F., Stalder M., Schnell L., Sommer B., Jucker M., Staufenbiel M. Abeta-induced inflammatory processes in microglia cells of APP23 transgenic mice. Am. J. Pathol. 158:2001;63-73.
10. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82:1991;239-259.
11. Brenneman D.E., Glazner G., Hill J.M., Hauser J., Davidson A., Gozes I. VIP neurotrophism in the central nervous system multiple effectors and identification of a femtomolar-acting neuroprotective peptide . Ann. N. Y. Acad. Sci. 865:1998;207-212.
12. Calhoun M.E., Wiederhold K.H., Abramowski D., Phinney A.L., Probst A., Sturchler-Pierrat C., Staufenbiel M., Sommer B., Jucker M. Neuron loss in APP transgenic mice. Nature. 395:1998;755-756.
13. Chan-Palay V., Lang W., Allen Y.S., Haesler U., Polak J.M. Cortical neurons immunoreactive with antisera against neuropeptide Y are altered in Alzheimer's-type dementia. J. Comp. Neurol. 238:1985;390-400.
14. Christensson-Nylander I., Herrera-Marschitz M., Staines W., Hökfelt T., Terenius L., Ungerstedt U., Cuello C., Oertel W.H., Goldstein M. Striato-nigral dynorphin and substance P pathways in the rat. I. Biochemical and immunohistochemical studies. Exp. Brain Res. 64:1986;169-192.
15. Coons A.H. Fluorescent antibody methods. Danielli J.F. General Cytochemical Methods. 1958;399-422 Academic Press, New York.
16. Costigan M., Befort K., Karchewski L., Griffin R.S., D'Urso D., Allchorne A., Sitarski J., Mannion J.W., Pratt R.E., Woolf C.J. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci. 3:2002;1-18.
17. Coumis U., Davies C.H. The effects of galanin on long-term synaptic plasticity in the CA1 area of rodent hippocampus. Neuroscience. 112:2002;173-182.
18. Crawley J.N. Galanin-acetylcholine interactions relevance to memory and Alzheimer's disease . Life Sci. 58:1996;2185-2199.
19. Darbarn D., Emson P.C. Neuropeptide Y-like immunoreactivity in neuritic plaques of Alzheimer's disease. Biochem. Biophys. Res. Commun. 126:1985;289-293.
20. Derrick B.E., Rodriguez S.B., Lieberman D.N., Martinez J.L. Jr. Mu opioid receptors are associated with the induction of hippocampal mossy fiber long-term potentiation. J. Pharmacol. Exp. Ther. 263:1992;725-733.
21. Dickson D.W., Farlo J., Davies P., Crystal H., Fuld P., Yen S.-H.C. Alzheimer's disease. A double-labeling immunohistochemical study of senile plaques. Am. J. Pathol. 132:1988;86-101.
22. Diez M., Koistinaho J., Kahn K., Games D., Hökfelt T. Neuropeptides in hippocampus and cortex in transgenic mice overexpressing V717F beta-amyloid precursor protein - initial observations. Neuroscience. 100:2000;259-286.
23. Ferrier J.N., Cross A.J., Johnson J.A., Roberts G.W., Crow T.J., Corsellis J.A.N., Lee Y.C., O'Shaughnessy D., Adrian T.E., McGregor B.P., Baracese-Hamilton A.J., Bloom S.R. Neuropeptides in Alzheimer type dementia. J. Neurol. Sci. 62:1983;159-170.
24. Franklin B.J., Paxinos G. The Mouse Brain in Stereotaxic Coordinates. 1997;Academic Press, San Diego.
25. Frey P. Cholecystokinin octapeptide (CCK 26-33), nonsulfated octapeptide and tetrapeptide (CCK 30-33) in rat brain analysis by high pressure liquid chromatography (HPLC) and radioimmunoassay (RIA) . Neurochem. Int. 5:1983;811-815.
26. Games D., Adams D., Alessandrini R., Barbour R., Berthelette P., Blackwell C., Carr T., Clemes 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., Wadworth S., Wolozin B., Zhao J. Alzheimer-type neuropathology in transgenic mice overexpressing V171F B-amyloid precursor protein. Nature. 373:1995;523-527.
27. Geula C., Mesulam M.M. Cholinergic systems and related neuropathological predilection patterns in Alzheimer's disease. Terry R.D., Katzman R., Blick K.L. Alzheimer's Disease. 1994;263-291 Raven Press, New York.
28. Glenner G.G., Wong C.W. Alzheimer's disease initial report of the purification and characterization of a novel cerebrovascular amyloid protein . Biochem. Biophys. Res. Commun. 120:1984;885-890.
29. Goate A., Chartier-Hallin M.-C., Mullan M., Brown J., Crawford F., Fidani L., Guiffra 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., Hardy J. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature. 349:1991;704-706.
30. Gottfries C.-G., Frederiksen S.O., Heilig M. Neuropeptides and Alzheimer's disease. Eur. Neuropsychopharmacol. 5:1995;491-500.
31. Hartman B.K., Zide D., Udenfriend S. The use of dopamine β-hydroxylase as a marker for the noradrenergic pathways of the central nervous system in the rat. Proc. Natl. Acad. Sci. USA. 69:1972;2722-2726.
32. Holmes F.E., Mahoney S., King V.R., Bacon A., Kerr N.C., Pachnis V., Curtis R., Priestly J.V., Wynick D. Targeted disruption of the galanin gene reduces the number of sensory neurons and their regenerative capacity. Proc. Natl. Acad. Sci. USA. 97:2000;11563-11568.
33. Hsiao K. Transgenic mice expressing Alzheimer amyloid precursor proteins. Exp. Gerontol. 33:1998;883-889.
34. Hökfelt T., Zhang X., Wiesenfeld-Hallin Z. Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci. 17:1994;22-30.
35. Hökfelt T., Ljungdahl Å., Fuxe K., Johansson O. Dopamine nerve terminals in the rat limbic cortex aspects of the dopamine hypothesis of schizophrenia . Science. 184:1974;177-179.
36. Hökfelt T, Liu H-X, Xu Z-QD, Diez M, Broberger C, Kopp J, Petersson S (2001) Neuropeptides and their receptors - distribution and expression under normal and disease conditions, in: New Frontiers of Neurotransmitter Research, Neuropeptides Update, Excerpta Medica, Japan, pp. 36-43.
37. Jacobs R.W., Farrivar N., Butcher L.L. Alzheimer dementia and reduced nicotinamide adenine dinucleotide (NADH)-diaphorase activity in senile plaques and the basal forebrain. Neurosci. Lett. 53:1985;39-44.
38. Johnson G.D., Nogueira Araujo G.M. A simple method of reducing the fading of immunofluorescence during microscopy. J. Immunol. Methods. 43:1981;349-350.
39. Kang J., Lemaire H.-G., Unterbeck A., Salbaum J.M., Master C.L., Grzeschik K.-H., Multhaup G., Beyreuther K., Müller-Hill B. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature. 325:1987;733-736.
40. Kelly P.H., Bondolfi L., Hunziker D., Schlecht H.P., Carver K., Maguire E., Abramowski D., Wiederhold K.H., Sturchler-Pierrat C., Jucker M., Bergmann R., Staufenbiel M., Sommer B. Progressive age-related impairment of cognitive behavior in APP23 transgenic mice. Neurobiol. Aging. 24:2003;365-378.
41. Kowall N.W., Beal M.F., Martin J.B. Neuropeptide Y, somatostatin and NADPH diaphorase reactive fibers contribute to senile plaque formation in Alzheimer's disease. Neurology. 36:1986;224.
42. Kuo Y.M., Kokjohn T.A., Beach T.G., Sue L.I., Brune D., Lopez J.C., Kalback W.M., Abramowski D., Sturchler-Pierrat C., Staufenbiel M., Roher A.E. Comparative analysis of amyloid-beta chemical structure and amyloid plaque morphology of transgenic mouse and Alzheimer's disease brains. J. Biol. Chem. 276:2001;12991-12998.
43. Lalonde R., Dumont M., Staufenbiel M., Sturchler-Pierrat C., Strazielle C. Spatial learning, exploration, anxiety, and motor coordination in female APP23 transgenic mice with the Swedish mutation. Brain Res. 956:2002;36-44.
44. Levy-Lahad E., Wasco W., Poorkaj P., Romano D.M., Oshima J., Pettingell W.H., Yu C., Jondro P.D., Schmidt S.D., Wang K., Crowley A.C., Fu Y.-H., Guenetter S.Y., Galas D., Nemens E., Wijsman E.M., Bird T.D., Schellenberg G.D., Tanzi R.E. Candidate gene for the chromosome 1 familial Alzheimer's disease locus. Science. 269:1995;973-977.
45. Ma W., Bisby M. Differential expression of galanin immunoreactivities in the primary sensory neurons following partial and complete sciatic nerve injuries. Neuroscience. 79:1997;1183-1195.
46. Maeda K., Kawata E., Sakai K., Chihara K. Effects of putative cognitive function-enhancing drugs and dopaminergic agents on somatostatin and neuropeptide Y in rat brain. Eur. J. Pharmacol. 233:1993;227-235.
47. Markey K.A., Kondo S., Shenkman L., Goldstein M. Purification and characterization of tyrosine hydroxylase from a clonal pheochromocytoma cell line. Mol. Pharmacol. 17:1980;79-85.
48. Marsh D., Grassi J., Vigny M., Massoulie J. An immunological study of rat acetylcholinesterase comparison with acetylcholinesterases from other vertebrates . J. Neurochem. 43:1984;204-213.
49. Masters C.L., Simms G., Winman N.A., Multhaup G., McDonald B.L., Beyreuther K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. USA. 82:1985;4245-4249.
50. Masters C.L., Multhaup G., Simms G., Pottgiesser J., Martins R.N., Beyreuther K. Neuronal origin of a cerebral amyloid neurofibrillary tangles of Alzheimer's disease contain the same protein as the amyloid of plaque cores and blood vessels . EMBO J. 4:1985;2757-2763.
51. Minthon L., Edvinsson L., Ekman R., Gustafson L. Neuropeptide levels in Alzheimer's disease and dementia with frontotemporal degeneration. J. Neural Transm. Suppl. 30:1990;57-67.
52. Moechars D., Dewachter I., Lorent K., Reverse D., Baekelandt V., Naidu A., Tesseur I., Spittaels K., Haute C.V., Checler F., Godaux E., Cordell B., Van Leuven F. Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J. Biol. Chem. 274:1999;6483-6492.
53. Morrison J.H., Rogers J., Scherr S., Benoit R., Bloom F.E. Somatostatin immunoreactivity in neuritic plaques of Alzheimer's patients. Nature. 314:1985;90-92.
54. Mufson J., Cochran E., Benzing W., Kordower J.H. Galaninergic innervation of the cholinergic vertical limb of the diagonal band (Ch2) and bed nucleus of the stria terminalis in aging, Alzheimer's disease and Down's syndrome. Dementia. 4:1993;237-250.
55. Mullan M., Crawford F., Axelman K., Houlden H., Lilius L., Winblad B., Lannfelt L. A pathogenic mutation for probable Alzheimer's disease in the APP gene at the N-terminus of beta-amyloid. Nat. Genet. 1:1992;345-347.
56. Nahin R.L., Ren K., de León M., Ruda M. Primary sensory neurons exhibit altered gene expression in a rat model of neuropathic pain. Pain. 58:1994;95-108.
57. Ögren S.O., Schött P.A., Kehr J., Yoshitake T., Misane I., Mannström P., Sandin J. Modulation of acetylcholine and serotonin transmission by galanin. Relationship to spatial and aversive learning. Ann. N. Y. Acad. Sci. 863:1998;342-363.
58. O'Meara G., Coumis U., Ma S.Y., Kehr J., Mahoney S., Bacon A., Allen S.J., Holmes F., Kahl U., Wang F.H., Kearns I.R., Ögren S.-O., Dawbarn D., Mufson E.J., Davies C., Dawson G., Wynick D. Galanin regulates the postnatal survival of a subset of basal forebrain cholinergic neurons. Proc. Natl. Acad. Sci. USA. 97:2000;11569-11574.
59. Paganetti P.A., Lis M., Klafki H.W., Staufenbiel M. Amyloid precursor protein truncated at any of the gamma-secretase sites is not cleaved to beta-amyloid. J. Neurosci. Res. 46:1996;283-293.
60. Palkovits M. Neuropeptide messenger plasticity in the CNS neurons following axotomy. Mol. Neurobiol. 10:1995;91-103.
61. Pease P.C. Buffered formaldehyde as a killing agent and primary fixative for electron microscopy. Anat. Rec. 142:1962;342.
62. Perry E.K., Tomlinson B.E., Blessed G., Perry R.H., Cross A.J., Crow T.J. Neuropathological and biochemical observations on the noradrenergic system in Alzheimer's disease. J. Neurol. Sci. 51:1981;279-287.
63. Phinney A.L., Deller T., Stalder M., Calhoun M.E., Frotscher M., Sommer B., Staufenbiel M., Jucker M. Cerebral amyloid induces aberrant axonal sprouting and ectopic terminal formation in amyloid precursor protein transgenic mice. J. Neurosci. 19:1999;8552-8559.
64. Platt J.L., Michael A.F. Retardation of fading and enhancement of intensity of immunofluorescence by p-phenylenediamine. J. Histochem. Cytochem. 31:1983;840-842.
65. Rogaev E.I., Sherrington E.A., Rogaeva E.A., Levesque G., Ikeda M., Liang Y., Chi H., LIn C., Holman K., Tsuda T., Mar L., Srobi S., Nacmias B., Placentini S., Amaducci L., Chumakov I., Cohen D., Lannfelt L., Fraser P.E., Rommens J.M., St George-Hyslop P.H. Familial Alzheimer's disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene. Nature. 376:1995;775-778.
66. Rossor M.N., Emson P.C., Iversen L.L., Mountjoy C.Q., Roth M., Hawthorn H., Ang V.T.Y., Jenkins J.S., Fahrenkrug J. Neuropeptides in senile dementia of Alzheimer type studies on somatostatin, vasoactive intestinal polypeptide and vasopressin . Clifford-Rose F. Metabolic Disorders of the Nervous System. 1981;418-420 Pitman, London.
67. Saunders A.M., Strittmatter W.J., Schmechel D., 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., Roses A.D. Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease. Neurology. 43:1993;1467-1472.
68. Schultzberg M., Hökfelt T., Terenius L., Elfvin L.G., Lundberg J.M., Brandt J., Elde R.P., Goldstein M. Enkephalin immunoreactive nerve fibres and cell bodies in sympathetic ganglia of the guinea-pig and rat. Neuroscience. 4:1979;249-270.
69. Schwartz J. Neurotransmitters as neurotrophic factors a new set of functions . Int. Rev. Neurobiol. 34:1990;1-23.
70. Selkoe D.J. The molecular pathology of Alzheimer's disease. Neuron. 6:1991;487-498.
71. Selkoe D.J. Translating cell biology into therapeutic advances in Alzheimer's disease. Nature. 399:1999;A23-A31.
72. Sheng J.G., Price D.L., Koliatsos V.E. Disruption of corticocortical connections ameliorates amyloid burden in terminal fields in a transgenic model of Abeta amyloidosis. J. Neurosci. 22:2002;9794-9799.
73. 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., St George-Hyslop P.H. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature. 375:1995;754-760.
74. Shi T.-J., Cui J.G., Meyerson B.A., Linderoth B., Hökfelt T. Regulation of galanin and dorsal horn in rat mononeuropathic models possible relation to tactile hypersensitivity . Neuroscience. 93:1999;741-757.
75. Stalder M., Phinney A., Probst A., Sommer B., Staufenbiel M., Jucker M. Association of microglia with amyloid plaques in brains of APP23 transgenic mice. Am. J. Pathol. 154:1999;1673-1684.
76. Steiner R.A., Hohmann J.G., Holmes A., Wrenn C.C., Cadd G., Jureus A., Clifton D.K., Luo M., Gutshall M., Ma S.Y., Mufson E.J., Crawley J.N. Galanin transgenic mice display cognitive and neurochemical deficits characteristic of Alzheimer's disease. Proc. Natl. Acad. Sci. USA. 98:2001;4184-4189.
77. Strand F.L., Rose K.J., Zuccarelli L.A., Kume J. Neuropeptide hormones as neurotrophic factors. Physiol. Rev. 71:1991;1017-1037.
78. Strittmatter W.J., Saunders A.M., Schmechel D., Pericak-Vance M., Enghild J., Slavesen G.S., 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. USA. 90:1993;1977-1981.
79. Strittmatter W.J., Wiesgraber K.H., Huang D.Y., Dong L.-M., Salvesen G.S., Pericak-Vance M., Schmechel D., Saunders A.M., Goldgaber D., Roses A.D. Binding of human apolipoprotein E to synthetic amyloid β peptide isoform-specific effects and implications for late-onset Alzheimer disease . Proc. Natl. Acad. Sci. USA. 90:1993;8098-8102.
80. Struble R.G., Powers R.E., Casanova M.F., Kitt C.A., Brown E.C., Price D.L. Neuropeptidergic systems in plaques of Alzheimer's disease. J. Neuropathol. Exp. Neurol. 46:1987;567-584.
81. Sturchler-Pierrat C., Staufenbiel M. Pathogenic mechanisms of Alzheimer's disease analyzed in the APP23 transgenic mouse model. Ann. N. Y. Acad. Sci. 920:2000;134-139.
82. Sturchler-Pierrat C., Abramowski D., Duke M., Wiederhold K.H., Mistl C., Rothacher S., Ledermann B., Burki K., Frey P., Paganetti P.A., Waridel C., Calhoun M.E., Jucker M., Probst A., Staufenbiel M., Sommer B. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc. Natl. Acad. Sci. USA. 94:1997;13287-13292.
83. Tanzi R.E., Kovacs D.M., Kim T.-W., Moir R.D., Guenette S.Y., Wasco W. The gene defects responsible for familial Alzheimer's disease. Neurobiol. Dis. 3:1996;159-168.
84. Theodorsson E., Rugarn O. Radioimmunoassay for rat galanin immunochemical and chromatographic characterization of immunoreactivity in tissue extracts . Scand. J. Clin. Lab. Invest. 60:2000;411-418.
85. Unger J.W., McNeill T.H., Lapham L.L., Hamill R.W. Neuropeptides and neuropathology in the amygdala in Alzheimer's disease relationship between somatostatin, neuropeptide Y and subregional distribution of neuritic plaques . Brain Res. 452:1988;293-302.
86. Van Dam D., D'Hooge R., Staufenbiel M., Van Ginneken C., Van Meir F., De Deyn P.P. Age-dependent cognitive decline in the APP23 model precedes amyloid deposition. Eur. J. Neurosci. 17:2003;388-396.
87. Wagner J.J., Terman G.W., Chaukin C. Endogenous dynorphins inhibit excitatory neurotransmission and block LTP induction in the hippocampus. Nature. 363:1993;451-454.
88. Wallin A., Carlsson A., Ekman R., Gottfries C.G., Karlsson I., Svennerholm L., Widerlöv E. Hypothalamic monoamines and neuropeptides in dementia. Eur. J. Neuropsychopharmacol. 1:1991;165-168.
89. Wang H., Sun H., Della Penna K., Benz R.J., Xu J., Gerhold D.L., Holder D.J., Koblan K.S. Chronic neuropathic pain is accompanied by global changes in gene expression and shares pathobiology with neurodegenerative diseases. Neuroscience. 114:2002;529-546.
90. Weber E., Evans C.J., Barchas J.D. Predominance of the amino-terminal octapeptide fragment of dynorphin in rat brain regions. Nature. 299:1982;77-79.
91. Weber E., Roth K.A., Barchas J.D. Immunohistochemical distribution of alpha-neo-endorphin/dynorphin neuronal systems in rat brain evidence for colocalization . Proc. Natl. Acad. Sci. USA. 79:1982;3062-3066.
92. Weisskopf M.G., Zalutsky R.A., Nicoll R.A. The opioid peptide dynorphin mediates heterosynapsic depression of hippocampal mossy fibre synapses and modulates long-term potentiation. Nature. 362:1993;423-427.
93. Widerlöv E., Wallin A., Gottfries C.G., Ekman R. Hypothalamic neuropeptides in neuropsychiatric illness. Genazzini A.R., Nappi G., Petraglia F., Martignoni E. Stress and Related Disorders, From Adaptation to Dysfunction, Parthenon. 1991;167-178 Carnforth, Lancashire.
94. Williams S.H., Johnston D. Actions of endogenous opioids on NMDA receptor-independent long-term potentiation in area CA3 of the hippocampus. J. Neurosci. 16:1996;3652-3660.
95. Xiao H.S., Huang Q.H., Zhang F.X., Bao L., Lu Y.J., Guo C., Yang L., Huang W.J., Fu G., Xu S.H., Cheng X.P., Yan Q., Zhu Z.D., Zhang X., Chen Z., Han Z.G. Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proc. Natl. Acad. Sci. USA. 99:2002;8360-8365.
96. Zamboni I., De Martino C. Buffered picric acid formaldehyde. A new rapid fixative for electron microscopy. J. Cell Biol. 35:1967;148A.
97. Zigmond R.E., Hyatt-Sachs H., Mohney R.P., Schreiber R.C., Shadiack A.M., Sun Y., Vaccariello S.A. Changes in neuropeptide phenotype after axotomy of adult peripheral neurons and the role of leukemia inhibitory factor. Persp. Dev. Neurobiol. 4:1996;75-90.