A comprehensive study of the spatiotemporal pattern of β-amyloid precursor protein mRNA and protein in the rat brain: Lack of modulation by exogenously applied nerve growth factor

Molecular Brain Research

Volumn 39, Issue 1-2, 1996, Pages 185-197

  Neve, Rachael L ^a   Valletta, Janice S ^b   Li, Yiwen ^b   Ventosa Michelman, Montserrat ^a   Holtzman, David M ^b,d   Mobley, William C ^b,c  

^a MCLEAN HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Gene expression; Nerve growth factor

Indexed keywords

AMYLOID BETA PROTEIN; MESSENGER RNA; NERVE GROWTH FACTOR; NEUROTROPHIC FACTOR; PROTEIN PRECURSOR; SERINE PROTEINASE INHIBITOR;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DOWN SYNDROME; EMBRYO DEVELOPMENT; FOREBRAIN; GENE EXPRESSION REGULATION; HUMAN; NERVE DEGENERATION; NONHUMAN; OLIGONUCLEOTIDE PROBE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT;

ANIMALIA; CRICETINAE;

EID: 0029892692     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/0169-328X(96)00007-1     Document Type: Article

References (67)

1. Anderson, J.P., Refolo, L.M., Wallace, W., Mehta, P., Krishnamurthi, M., Gotlib, J., Bierer, L., Haroutunian, V., Perl, D. and Robakis, N.K., Differential brain expression of the Alzheimer's amyloid precursor protein, EMBO J., 8 (1989) 3627-3632.
2. Chirgwin, J.M., Przybla, A.E., MacDonald, R.J. and Rutter, W.J., Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease, Biochemistry, 18 (1979) 5294-5299.
3. Cohen, M.L., Golde, T.E., Usiak, M.F., Younkin, L.H. and Younkin, S.G., In situ hybridization of nucleus basalis neurons shows increased β-amyloid mRNA in Alzheimer disease, Proc. Natl. Acad. Sci. USA, 85 (1988) 1227-1231.
4. Danielson, P.E., Forss-Petter, S., Brow, M.A., Calavetta, L., Douglass, J., Milner, R., Sutcliffe, J.G., p1B15: a cDNA clone of the rat mRNA encoding cyclophilin, DNA, 7 (1988) 261-267.
5. Fischer, W., Wictorin, K., Bjorklund, 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 (Lond.), 329 (1987) 65-68.
6. Fisher, S., Gearhart, J.D. and Oster-Granite, M.L., Expression of the amyloid precursor protein gene in mouse oocytes and embryos, Proc. Natl. Acad. Sci. USA, 88 (1991) 1779-1782.
7. Forloni, G., Del Bo, R., Angeretti, N., Smiroldo, S., Gabellini, N. and Vantini, G., Nerve growth factor does not influence the expression of β amyloid precursor protein mRNA in rat brain: in vivo and in vitro studies, Brain Res., 620 (1993) 292-296.
8. Fukuchi, K., Kamino, K., Deeb, S.S., Smith, A.C., Dang, T. and Martin, G.M., Overexpression of amyloid precursor protein alters its normal processing and is associated with neurotoxicity, Biochem. Biophys. Res. Comm., 182 (1992) 165-173.
9. Fukuyama, R., Chandrasekaran, K. and Rapaport, S.I., Nerve growth factor-induced neuronal differentiation is accompanied by differential induction and localization of the amyloid precursor protein (APP) in PC12 cells and variant PC12S cells, Mol. Brain Res., 17 (1993) 17-22.
10. 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, Ivan, Little, S., Masliah, E., McConlogue, L., Montoya-Zavala, 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 (1995) 523-527.
11. Glenner, G.G., Alzheimer's disease: the commonest form of amyloidosis, Arch. Pathol. Lab. Med. 107 (1983) 281-282.
12. Gnahn, H., Hefti, F., Heumann, R., Schwab, M.E. and Thoenen, H., NGF-mediated increase of choline acetyltransferase (ChAT) in the neonatal rat forebrain: evidence for a physiological role of NGF in the brain?, Dev. Brain Res., 9 (1983) 42-52.
13. Golde, T.E., Estus, S., Usiak, M., Younkin, L.H. and Younkin, S.G., Expression of β amyloid protein precursor mRNAs: recognition of a novel alternatively spliced form and quantitation in Alzheimer's disease using PCR, Neuron, 4 (1990) 253-267.
14. Golde, T.E., Estus, S., Younkin, L.H., Selkoe, D.J. and Younkin, S.G., Processing of the amyloid protein precursor to potentially amyloidogenic derivatives, Science, 55 (1992) 728-730.
15. Goldgaber, D., Harris, H.W., Hla, T., Maciag, T., Donnelly, R.J., Jacobsen, J.S., Vitek, M.P. and Gajdusek, D.C., Interleukin 1 regulates synthesis of amyloid β-protein precursor mRNA in human endothelial cells, Proc. Natl. Acad. Sci. USA, 86 (1989) 7606-7610.
16. Griffin, W.S.T., Stanley, L.C., Ling, C., White, L., MacLeod, V., Perrot, L.J., White, C.L., III and Araoz, C., Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease, Proc. Natl. Acad. Sci. USA, 86 (1989) 7611-7615.
17. Hagg, T., Hagg, F., Vahlsing, H.L., Manthorpe, M. and Varon, S., Nerve growth factor effects on cholinergic neurons of neostriatum and nucleus accumbens in the adult rat, Neuroscience, 30 (1989) 95-103.
18. Hefti, F., Nerve growth factor (NGF) promotes survival of septal cholinergic neurons after fimbrial transection, J. Neurosci., 6 (1986) 2155-2162.
19. Higgins, G.A., Oyler, G.A., Neve, R.L., Chen, K.S. and Gage, F.H., Altered levels of amyloid protein precursor transcripts in the basal forebrain of behaviorally impaired aged rats, Proc. Natl. Acad. Sci. USA, 87 (1990) 3032-3036.
20. Higgins, L.S., Holtzman, D.M., Rabin, J., Mobley, W.C. and Cordell, B., Transgenic mouse brain histopathology resembles early Alzheimer's disease, Ann. Neurol., 35 (1994) 598-607.
21. Holtzman, D.M., Bayney, R.M., Li, Y., Khosrovi, H., Berger, C.N., Epstein, C.J. and Mobley, W.C., Dysregulation of gene expression in mouse trisomy 16, an animal model of Down syndrome, EMBO J., 11 (1992) 619-627.
22. trk mRNA marks NGF-responsive forebrain neurons: evidence that trk gene expression is induced by NGF, Neuron, 9 (1992) 465-478.
23. Holtzman, D.M., Li, Y., Chen, K., Gage, F.H., Epstein, C.J. and Mobley, W.C., Nerve growth factor reverses neuronal atrophy in a Down syndrome model of age-related neurodegeneration, Neurology, 43 (1993) 2668-2673.
24. Johnson, S.A., McNeill, T., Cordell, B. and Finch, C.E., Relation of neuronal APP-KPI/APP-695 mRNA ratio and neuritic plaque density in Alzheimer's disease, Science, 248 (1990) 854-857.
25. Johnston, M.V., Rutkowski, J.L., Wainer, B.H., Long, J.B. and Mobley, W.C., NGF effects on developing forebrain cholinergic neurons are regionally specific, Neurochem. Res., 12 (1987) 985-994.
26. Kang, J. and Müller-Hill, B., The sequence of the two extra exons in rat preA4, Nucl. Acids Res., 17 (1989) 2130.
27. 695 mRNA is predominantly produced in rat and human brain, Biochem. Biophys. Res. Commun., 166 (1990) 1192-1200.
28. Koliatsos, V.E., Clatterbuck, R.E., Nauta, H.J., Knusel, B., Burton, L.E., Hefti, F.F., Mobley, W.C., Price, D.L., Human nerve growth factor prevents degeneration of basal forebrain cholinergic neurons in primates, Ann. Neurol., 30 (1991) 831-840.
29. Löffer, J. and Huber, G., β-amyloid precursor protein isoforms in various rat brain regions and during brain development, J. Neurochem., 59 (1992) 1316-1324.
30. Malamud, N., Neuropathology of organic brain syndromes associated with aging. In: C.M. Gaitz (Ed.), Aging and the Brain, 3rd edn., Plenum Publ., New York, 1972, pp. 63-87.
31. Mobley, W.C., Rutkowski, J.L., Tennekoon, S.J., Buchanan, K. and Johnston, M.V., Choline acetyltransferase in striatum of neonatal rats increased by nerve growth factor, Science, 229 (1985) 284-287.
32. Mobley, W.C., Rutkowski, J.L., Tennekoon, G.E., Gemski, J., Buchanan, K. and Johnston, M.V., Nerve growth factor increases choline acetyltransferase activity in developing basal forebrain neurons, Mol. Brain Res., 387 (1986) 53-62.
33. Mobley, W.C., Neve, R.L., Prusiner, S.B., McKinley, M.P., Nerve growth factor increases mRNA levels for the prion protein and the β-amyloid protein precursor in the developing hamster brain, Proc. Natl. Acad. Sci. USA, 85 (1988) 9811-9815.
34. Mobley, W.C., Barrall, T., Gwag, B.J. and Springer, J.E., Developmental expression of nerve growth factor (NGF) receptor mRNA in the rat basal forebrain: influence of NGF administration, Soc. Neurosci. Abst., 16 (1990) 297.
35. Moran, P.M., Higgins, L.S., Cordell, B. and Moser, P.C., Age-related learning deficits in transgenic mice expressing the 751-amino acid isoform of human β-amyloid precursor protein, Proc. Natl. Acad. Sci. USA, 92 (1995) 5341-5345.
36. Neve, R.L., Harris, P., Kosik, K.S., Kurnit, D.M. and Donlon, T.A., Identification of cDNA clones for the human microtubule-associated protein tau and chromosomal localization of the genes for tau and microtubule-associated protein 2, Mol. Brain Res., 1 (1986) 271-280.
37. Neve, Rachael L., Finch, E.A. and Dawes, L.R., Expression of the Alzheimer amyloid precursor gene transcripts in the human brain, Neuron, 1 (1988) 669-677.
38. Neve, Rachael L., Rogers, J., Higgins, F.A., The Alzheimer amyloid precursor-related transcript lacking the β/A4 sequence is specifically increased in Alzheimer disease brain, Neuron, 5 (1990) 329-338.
39. O'Hara, B.F., Fisher, S., Oster-Granite, M.L., Gearhart, J.D. and Reeves, R.H., Developmental expression of the amyloid precursor protein, growth-associated protein 43, and somatostatin in normal and trisomy 16 mice, Dev. Brain Res., 49 (1989) 300-304.
40. Ohyagi, Y., and Tabira, T., Effect of growth factors and cytokines on expression of amyloid β protein precursor mRNAs in cultured neural cells, Mol. Brain Res., 18 (1993) 127-132.
41. Oltersdorf, T., Ward, P.J., Henriksson, T., Beattie, E.C., Neve, R., Lieberbug, I. and Fritz, L.C., The Alzheimer amyloid precursor protein: identification of a stable intermediate in the biosynthetic/degradative pathway, J. Biol. Chem., 265 (1990) 4492-4497.
42. Oster-Granite, M.L. and Herndon, R.M., The development of the cerebellar cortex of the Syrian hamster, Mesocricetus auratus. Foliation, cytoarchitectonic, Golgi, and electron microscopic studies, J. Comp. Neurol., 169 (1976) 443-479.
43. Palmert, M.R., Golde, T.E., Cohen, M.L., Kovacs, D.M., Tanzi, R.E., Gusella, J.F., Usiak, M.F., Younkin, L.H. and Younkin, S.G., Amyloid protein precursor messenger RNAs: differential expression in Alzheimer's disease, Science, 241 (1988) 1080-1082.
44. Price, D.L., Koliatsos, V.E., Sisodia, S.S., Koo, E.H., Martin, L.J., Walker, L.C., Appelgate, M.D. and Cork, L.C., Amyloid-related proteins and nerve growth factor in Alzheimer's disease and animal models, Clin. Neuropharmacol., 14, Suppl. 1 (1991) S9-S14.
45. Price, D.L., Martin, L.J., Sisodia, S.S., Wagster, M.V., Koo, E.H., Walker, L.C., Koliatsos, V.E. and Cork, L.C., Aged non-human primates: an animal model of age-associated neurodegenerative disease, Brain Pathol., 1 (1991) 287-296.
46. Quon, D., Wang, Y., Catalano, R., Scardina, J.M., Murakami, K. and Cordell, B., Formation of β-amyloid protein deposits in brains of transgenic mice, Nature, 352 (1991) 239-241.
47. Refolo, L.M., Salton, S.R.J. anderson, J.P., Mehta, P. and Robakis, N.K., Nerve and epidermal growth factors induce the release of the Alzheimer amyloid precursor from PC12 cells, Biochem. Biophys. Res. Commun., 164 (1989) 664-670.
48. Schneider, G.E., Early lesions of superior colliculus: factors affecting the formation of abnormal retinal projections, Brain Behav. Evol., 8 (1973) 73-109.
49. Schubert, D., Jin, L.-W., Saitoh, T. and Cole, G., The regulation of amyloid β protein secretion and its modulatory role in cell adhesion, Neuron, 3 (1989) 689-694.
50. Selkoe, D.J., Podlisny, M.B., Joachim, C.L., Vickers, E.A., Lee, G., Fritz, L.C. and Oltersdorf, T., β-Amyloid precursor protein of Alzheimer disease occurs as 110-135-kilodalton membrane-associated proteins in neural and nonneural tissue, Proc. Natl. Acad. Sci. USA 85 (1988) 7341-7345.
51. Shivers, B.D., Hilbich, C., Multhaup, G., Salbaum, M., Beyreuther, K. and Seeburg, P.H., Alzheimer's disease amyloidogenic glycoprotein: expression pattern in rat brain suggests a role in cell contact, EMBO J., 7 (1988) 1365-1370.
52. Siman, R., Card, J.P., Nelson, R.B. and Davis, L.G., Expression of β-amyloid precursor protein in reactive astrocytes following neuronal damage, Neuron, 3 (1980) 275-285.
53. Smith, C.J., Wion, D. and Brachet, P., Nerve growth factor-induced neuronal differentiation is accompanied by differential splicing of β-amyloid precursor mRNAs in the PC12 cell line, Mol. Brain Res., 10 (1991) 351-354.
54. Smith, C.J., Johnson, E.M., Jr., Osborne, P., Freeman, R.S., Neveu, I. and Brachet, P., NGF deprivation and neuronal degeneration trigger altered β-amyloid precursor protein gene expression in the rat superior cervical ganglia in vivo and in vitro, Mol. Brain Res., 17 (1993) 328-334.
55. Springer, J.E., Robbins, E., Meyer, S., Baldino, F.J. and Lewis, M.E., Localization of nerve growth factor receptor mRNA in the rat basal forebrain with in situ hybridization histochemistry, Cell. Mol. Neurobiol., 10 (1990) 33-39.
56. Tanaka, S., Shiojiri, S., Takahashi, Y., Kitaguchi, N., Ito, H., Kameyama, M., Kimura, J., Nakamura, S. and Ueda, K., Tissue-specific expression of three types of β-protein precursor mRNA: enhancement of protease inhibitor-harboring types in Alzheimer's disease brain, Biochem. Biophys. Res. Commun., 165 (1989) 1406-1414.
57. Terry, R.D., Maslia, E., Salmon, D.P., Butters, N., DeTeresa, R., Hill, R., Hansen, L.A. and Katzman, R., Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment, Ann. Neurol., 30 (1991) 572-580.
58. Terry, R.D., Peck, A., DeTeresa, R., Schlechter, R. and Horoupian, D.S., Some morphometric aspects of the brain in senile dementia of the Alzheimer type, Ann. Neurol., 10 (1983) 184-192.
59. Van Nostrand, W.E., Farrow, J.S., Wagner, S.L., Bhasin, R., Goldgaber, D., Cotman, C.W. and Cunningham, D.D., The predominant form of the amyloid β-protein precursor in human brain is protease nexin 2, Proc. Natl. Acad. Sci. USA, 88 (1991) 10302-10306.
60. Wallace, W.C., Bragin, V., Robakis, N.K., Sambamurti, K., Vander-Puttern, D., Merrill, C.R., Davis, K.L., Santucci, A.C. and Haroutunian, V., Increased biosynthesis of Alzheimer amyloid precursor protein in the cerebral cortex of rats with lesions of the nucleus basalis of Meynert, Mol. Brain Res., 10 (1991) 173-178.
61. Wasco, W., Bupp, K., Magendantz, M., Gusella, J.F., Tanzi, R.E. and Solomon, F., Identification of a mouse brain cDNA that encodes a protein related to the Alzheimer disease-associated amyloid β protein precursor, Proc. Natl. Acad. Sci. USA, 89 (1992) 10758-10762.
62. Wasco, W., Gurubhagavatula, S., Paradis, M.d., Romano, D.M., Sisodia, S.S., Hyman, B.T., Neve, R.L. and Tanzi, R.E., Isolation and characterization of APLP2 encoding a homologue of the Alzheimer's associated amyloid β protein precursor, Nature Genet., 5 (1993) 95-100.
63. Whitehouse, P.J., Price, D.L., Struble, R.G., Clark, A.W., Coyle, J.T., DeLong, M.R., Alzheimers disease and senile dementia: loss of neurons in the basal forebrain, Science, 215 (1982) 1237-1239.
64. Williams, L.R., Varon, S., Peterson, G.M., Wictorin, K., Fischer, W., Bjorklund, A. and Gage, F.H., Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbriafornix transection, Proc. Natl. Acad. Sci. USA, 83 (1986) 9231-9235.
65. Yamada, T., Sasaki, H., Furuya, H., Miyata, T., Goto, I. and Sasaki, Y., Complementary DNA for the mouse homolog of the human amyloid beta protein precursor, Biochem. Biophys. Res. Commun., 149 (1987) 665-671.
66. Yoshikawa, K., Aizawa, T. and Hayashi, Y., Degeneration in vitro of post-mitotic neurons overexpressing the Alzheimer amyloid protein precursor, Nature, 359 (1992) 64-67.
67. Zhou, J., Valletta, J.S., Grimes, M.L. and Mobley, W.C., Multiple levels of regulation of TrkA in PC12 cells by nerve growth factor, J. Neurochem., 65 (1995) 1146-1156.