Down-regulation of the amyloid protein precursor of Alzheimer's disease by antisense oligonucleotides reduces neuronal adhesion to specific substrata

Brain Research

Volumn 770, Issue 1-2, 1997, Pages 72-80

  Coulson, Elizabeth J ^a,b,c   Barrett, Graham L ^c   Storey, Elsdon ^a,b   Bartlett, Perry F ^c,d   Beyreuther, Konrad ^e   Masters, Colin L ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d The CRC for Cellular Growth Factors   (Australia)

^e UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Collagen; Fibronectin; Heparan sulphate proteoglycan; Laminin; Murine

Indexed keywords

AMYLOID PRECURSOR PROTEIN; ANTISENSE OLIGODEOXYNUCLEOTIDE;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL CELL; ARTICLE; CELL ADHESION; DOWN REGULATION; EXTRACELLULAR MATRIX; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANIMALS, NEWBORN; ANTISENSE ELEMENTS (GENETICS); CELL ADHESION; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; CULTURE MEDIA; EXTRACELLULAR MATRIX; GANGLIA, SPINAL; MICE; NEURITES; NEURONS; OLIGONUCLEOTIDE PROBES;

EID: 0030727343     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(97)00757-9     Document Type: Article

References (78)

1. Allinquant B., Mailleux P., Moya K., Bouillot C., Prochiantz A. Down regulation of amyloid protein precursor inhibits neurite outgrowth in vitro. J. Cell. Biol. 128:1995;919-927.
2. Araki W., Kitaguchi N., Tokushima Y., Ishii K., Aratake H., Shimohama S., Nakamura S., Kimura J. Trophic effect of β-amyloid precursor protein on cerebal cortical neurons in culture. Biochem. Biophys. Res. Commun. 181:1991;265-271.
3. Barrett G.L., Bartlett P.F. The p75 nerve growth factor receptor mediates survival or death depending on the stage of sensory neuron development. Proc. Natl. Acad. Sci. USA. 91:1994;6501-6505.
4. Beher D., Hesse L., Masters C.L., Beyreuther K. Regulation of amyloid precursor protein (APP)-binding to collagen and mapping of the binding sites on APP and collagen type I. J. Biol. Chem. 271:1996;1613-1620.
5. J.E. Bottenstein, Growth and differentiation of neural cells in defined media, in: J.E. Bottenstein, G. Sato (Eds.), Cell Culture in the Neurosciences, Plenum Press, New York, 1979, pp. 3-21.
6. Breen K.C., Bruce M., Anderton B.H. Beta amyloid precursor protein mediates neuronal cell-cell and cell-surface adhesion. J. Neurosci. Res. 28:1991;90-110.
7. Breen K.C. APP-collagen interaction is mediated by a heparin bridge mechanism. Mol. Chem. Neuropathol. 16:1992;109-121.
8. Bush A.I., Martins R.N., Rumble B., Moir R., Fuller S., Milward E., Currie J., Ames D., Weidemann A., Fischer P., Multhaup G., Beyreuther K., Masters C.L. The amyloid precursor protein of Alzheimer's disease is released by human platelets. J. Biol. Chem. 265:1992;15977-15983.
9. Chang P.L., Isaacs K.R. Synapse formation occurs in association with the induction of long-term potentiation in two-year-old rat hippocampus in vitro. Neurobiol. Aging. 12:1991;517-522.
10. Checler F. Processing of the β amyloid precursor protein and its regulation in Alzheimer's disease. J. Neurochem. 65:1995;1431-1444.
11. Chen M., Yankner B.A. An antibody to β amyloid and the amyloid precursor protein inhibits cell-substratum adhesion in many mammalian cell types. Neurosci. Lett. 125:1991;223-226.
12. David G. Integral membrane heparan sulphate proteoglycans. FASEB J. 7:1993;1023-1030.
13. Douville P.J., Harvey W.J., Carbonetto S. Isolation and partial charaterization of high affinity laminin receptors in neural cells. J. Biol. Chem. 263:1988;14964-14969.
14. Evin G., Beyreuther K., Masters C.L. Alzheimer's disease amyloid precursor protein (AβPP): proteolytic processing, secretases and βA4 amyloid production. Amyloid: Int. J. Exp. Clin. Invest. 1:1994;263-280.
15. Furukawa K., Barger S.W., Blalock E.M., Mattson M.P. Activation of potassium channels and suppression of neuronal activity by secreted β-amyloid-precursor protein. Nature. 379:1996;74-78.
16. Gaëta B.A. Database similarity searching using BLAST and FastA. Austral. Biotechnol. 5:1995;282-290.
17. Gee S.H., Blacher R.W., Douville P.J., Provost P.R., Yurchenoco P.D., Carbonetto S. Laminin-binding protein 120 from brain is closely related to the dystrophin-associated glycoprotein, dystroglycan, and binds with high affinity to the major heparin binding domain of laminin. J. Biol. Chem. 268:1993;1472-14980.
18. Ghiso J., Tagliavini F., Timmers W.F., Frangione B. Alzheimer's disease amyloid precursor protein is present in senile plaques and cerebrospinal fluid: immunohistochemical and biochemical characterization. Biochem. Biophys. Res. Commun. 163:1989;430-437.
19. Ghiso J., Rostagno A., Gardella J.E., Liem L., Gorevic P.D., Frangione B. A 109-amino-acid C-terminal fragment of Alzheimer's-disease amyloid precursor protein contains a sequence -RHDS- that promotes cell adhesion. Biochem. J. 288:1992;1053-1059.
20. 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.
21. Golde T.E., Estus S., Usiak M., Younkin L.H., 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.
22. Halfter W. A heparan sulphate proteoglycan in developing avian axonal tracts. J. Neurosci. 13:1993;2863-2873.
23. Hilbich C., Mönning U., Grund C., Masters C.L., Beyreuther K. Amyloid-like properties of peptides flanking the epitope of amyloid precursor protein-specific monoclonal antibody 22C11. J. Biol. Chem. 268:1993;26571-26577.
24. Hunter A.J., Leslie R.A., Gloger I.S., Lawrence M. Probing the function of novel genes in the nervous system: is antisense the answer? Trends Neurosci. 18:1995;329-331.
25. Jin L.W., Ninomiya H., Roch J.M., Schubert D., Masliah E., Otero D.A., Saitoh T. Peptides containing the RERMS sequence of amyloid β/A4 protein precursor bind cell surface and promote neurite extension. J. Neurosci. 14:1994;5461-5470.
26. Jucker M., Walker L.C., Kibbey M.C., Kleinman H.K., Ingram D.K. Localization of a laminin-binding protein in brain. Neuroscience. 56:1993;1009-1022.
27. Kaas J.H. Plasticity of sensory and motor maps in adult mammals. Annu. Rev. Neurosci. 14:1991;137-167.
28. Kang J., Lemaire H., Unterbeck A., Salbaum J.M., Masters C.L., Grzeschik K., 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.
29. Kibbey M.C., Jucker M., Weeks B.S., Neve R.L., Van Nostrand W.E., Kleinman H.K. β-Amyloid precursor protein binds to the neurite-promoting IKVAV site of laminin. Proc. Natl. Acad. Sci. USA. 90:1993;10150-10153.
30. Kitaguchi N., Takahashi Y., Tokushima Y., Shiojiri S., Ito H. Novel precursor of Alzheimer's disease amyloid protein shows protease inhibitory activity. Nature. 331:1988;530-532.
31. Koo E.H., Sisodia S.S., Archer D.R., Martin L.J., Weidemann A., Beyreuther K., Fischer P., Masters C.L., Price D.L. Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc. Natl. Acad. Sci. USA. 87:1990;1561-1565.
32. Koo E.H., Park L., Selkoe D.J. Amyloid β-protein as a substrate interacts with extracellular matrix to promote neurite outgrowth. Proc. Natl. Acad. Sci. USA. 90:1993;4748-4752.
33. König G., Mönning U., Czech C., Prior R., Banati R., Schreiter-Gasser U., Bauer J., Masters C.L., Beyreuther K. Identification and differential expression of a novel alternative splice isoform of the βA4 amyloid precursor protein (APP) mRNA in leukocytes and brain microglial cells. J. Biol. Chem. 267:1992;10804-10809.
34. LeBlanc A.C., Kovacs D.M., Chen H.Y., Villaré F.F., Tykocinski M., Autilio-Gambetti L., Gambetti P. Role of amyloid precursor protein (APP): study with antisense transfection of human neuroblastoma cells. J. Neurosci. Res. 31:1992;635-645.
35. 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.
36. + homoeostasis in Alzheimer's disease. Trends Neurosci. 16:1993;409-414.
37. Mattson M.P. Secreted forms of β-amyloid precursor protein modulate dendrite outgrowth and calcium responses to glutamate in cultured embryonic hippocampal neurons. J. Neurobiol. 25:1994;439-450.
38. Milward E., Papadopoulos R., Fuller S.J., Moir R.D., Small D., Beyreuther K., Masters C.L. The amyloid protein precursor of Alzheimer's disease is a mediator of the effects of nerve growth factor on neurite outgrowth. Neuron. 9:1992;129-137.
39. 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 developing hamster brain. Proc. Natl. Acad. Sci. USA. 85:1988;9811-9815.
40. Multhaup G., Bush A.I., Pollwein P., Masters C.L. Interaction between the zinc(II) and the heparin binding site of the Alzheimer's disease βA4 amyloid precursor protein (APP). FEBS Lett. 355:1994;151-154.
41. Murphy M., Reid K., Brown M.A., Bartlett P.F. Involvement of leukemia inhibitory factor and nerve growth factor in the development of dorsal root ganglion neuron. Development. 117:1993;1173-1182.
42. Mönning U., Sandbrink R., Banati R.B., Masters C.L., Beyreuther K. Transforming growth factor β mediates increase of mature transmembrane amyloid precursor protein in microglial cells. FEBS Lett. 342:1994;267-272.
43. Müller U., Cristina N., Li Z.-W., Wolfer D.P., Lipp H.-P., Rülicke T., Brandner S., Aguzzi A., Weissmann C. Behavioral and anatomical deficits in mice homozygous for a modified β-amyloid precursor protein gene. Cell. 79:1994;755-765.
44. Narindrasorasak S., Lowery D., Gonzalez-DeWhitt P., Poorman R.A., Greenberg B., Kisilevsky R. High affinity interactions between the Alzheimer's β-amyloid precursor proteins and the basement membrane form of heparan sulphate proteoglycan. J. Biol. Chem. 266:1991;12878-12883.
45. Narindrasorasak S., Lowery D.E., Altman R.A., Gonzalez-De Whitt P.A., Greenberg B.D., Kisilevsky R. Characterization of high affinity binding between laminin and Alzheimer's disease amyloid precursor proteins. Lab. Invest. 67:1992;643-652.
46. Nurcombe V., Ford M.D., Wildschut J.A., Bartlett P.F. Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulphate proteoglycan. Science. 260:1993;103-106.
47. Ohyagi Y., Takahashi K., Kamegai M., Tabira T. Developmental and differential expression of beta amyloid protein precursor mRNAs in mouse brain. Biochem. Biophys. Res. Commun. 167:1990;54-60.
48. Oltersdorf T., Ward P.J., Henriksson T., Beattie E.C., Neve R., Lieberburg I., 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.
49. Pangalos M.N., Efthimiopoulos S., Shioi J., Robakis N.K. The chondroitin sulphate attachment site of appican is formed by splicing out exon 15 of the amyloid precursor gene. J. Biol. Chem. 270:1995;10388-10391.
50. Ponte P., Gonzalez-DeWhitt P., Schilling J., Miller J., Hsu D., Greenberg B., Davis K., Wallace W., Lieberburg I., Fuller F., Cordell B. A new A4 amyloid mRNA contains a domain homologous to serine proteinase inhibitors. Nature. 331:1988;525-527.
51. Price D.L., Sisodia S.S., Gandy S.E. Amyloid beta amyloidosis in Alzheimer's disease. Curr. Opin. Neurol. 8:1995;268-274.
52. Qiu W.Q., Ferreira A., Miller C., Koo E.H., Selkoe D.J. Cell-surface β-amyloid precursor protein stimulates neurite outgrowth of hippocampal neurons in an isoform-dependent manner. J. Neurosci. 15:1995;2157-2167.
53. Quattrone A., Di Pasquale G., Capaccioli S. Enhancing antisense oligonucleotides intracellular levels by means of cationic lipids as vectors. Biochemica. 1:1995;25-29.
54. Raghow R. Regulation of messenger RNA turnover in eukaryotes. Trends Biochem. Sci. 12:1987;358-360.
55. Saitoh T., Sundsmo M., Roch J.M., Kumura N., Cole G., Schubert D., Oltersdorf T., Schenk D.B. Secreted form of amyloid-β protein precursor is involved in the growth regulation of fibroblasts. Cell. 58:1989;615-622.
56. Sandbrink R., Masters C.L., Beyreuther K. Similar alternative splicing of a non-homologous domain in βA4-amyloid protein precursor-like proteins. J. Biol. Chem. 269:1994;14227-14234.
57. Sandbrink R., Masters C.L., Beyreuther K. betaA4-amyloid protein precursor mRNA isoforms without exon 15 are ubiquitously expressed in rat tissues including brain but not in neurons. J. Biol. Chem. 269:1994;1510-1517.
58. Schubert D., LaCorbiere M., Saitoh T., Cole G. Characterization of an amyloid β precursor protein that binds heparin and contains tyrosine sulphate. Proc. Natl. Acad. Sci. USA. 86:1989;2066-2069.
59. Schubert D., Behl C. The expression of amyloid beta protein precursor protects nerve cells from beta-amyloid and glutamate toxicity and alters their interaction with the extracellular matrix. Brain Res. 629:1993;275-282.
60. Selkoe D.J. Cell biology of the amyloid β-protein precursor and the mechanism of Alzheimer's disease. Ann. Rev. Cell Biol. 10:1994;373-403.
61. Simons M., Ikonen E., Tiennari P.J., Cid-Arregui A., Mönning U., Beyreuther K., Dotti C.G. Intracellular routing of human amyloid protein precursor: axonal delivery followed by transport to the dendrites. J. Neurosci. 41:1995;121-128.
62. Small D.H., Nurcombe V., Moir R., Michaelson S., Monard D., Beyreuther K., Masters C.L. Association and release of the amyloid protein precursor of Alzheimer's disease from chick brain extracellular matrix. J. Neurosci. 12:1992;4143-4150.
63. Small D.H., Nurcombe V., Reed G., Clarris H., Moir R., Beyreuther K., Masters C.L. A heparin-binding domain in the amyloid protein precursor of Alzheimer's disease is involved in the regulation of neurite outgrowth. J. Neurosci. 14:1994;2117-2127.
64. a-inhibitor, a form of Alzheimer amyloid precursor protein. Science. 248:1990;1126-1128.
65. E. Storey, K. Beyreuther, C.L. Masters, Alzheimer's disease amyloid precursor protein on the surface of cortical neurons in primary culture co-localizes with adhesion patch components, Brain Res. 735 (1996) 217-231.
66. E. Storey, T. Spurck, J. Pickett-Heaps, K. Beyreuther, C.L. Masters, The amyloid precursor protein of Alzheimer's disease is found on the surface of static but not actively motile portions of neurites, Brain Res. 735 (1996) 59-66.
67. Tanzi R.E., McClatchey A.I., Lamperti D., Villa-Komaroff L., Gusella J.F., Neve R.L. Protease inhibitor domain encoded by an amyloid protein precursor mRNA associated with Alzheimer's disease. Nature. 331:1988;528-530.
68. Thinakaran G., Kitt C.A., Roskams A.J.I., Slunt H.H., Masliah E., Von Koch C., Ginsberg S.D., Ronnett G.V., Reed R.R., Price D.L., Sisodia S.S. Distribution of an APP homologue, APLP2, in the mouse olfactory system: A potential role for APLP2 in axogenisis. J. Neurosci. 15:1995;6314-6326.
69. Venstrom K.A., Reichardt L.F. Extracellular matrix 2: role of extracellular matrix molecules and their receptors in the nervous system. FASEB J. 7:1993;996-1003.
70. Wagner R.W. Gene inhibition using antisense oligodeoxynucleotides. Nature. 372:1994;333-335.
71. Wasco W., Bupp K., Magendantz M., Gusella J.F., Tanzi R.E., 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.
72. Wasco W., Gurubhagavatula S., Paradis M.D., Romano D.M., Sisodia S.S., Hyman B.T., Neve R.L., Tanzi R.E. Isolation and characterization of APLP2 encoding a homologue of the Alzheimer's associated amyloid β protein precursor. Nat. Genet. 5:1993;95-100.
73. Weidemann A., König G., Bunke D., Fischer P., Salbaum J.M., Masters C.L., Beyreuther K. Identification, biogenesis and localization of precursors of Alzheimer's disease A4 amyloid protein. Cell. 57:1989;115-126.
74. Wolff J.M., Frank R., Mujoo K., Spiro R.C., Reisfled R.A., Rathjen F.G. A human brain glycoprotein related to the mouse cell adhesion molecule L1. J. Biol. Chem. 263:1988;11943-11947.
75. Woolf T.M., Melton D.A., Jennings C.G.B. Specificity of antisense oligonucleotide. Proc. Natl. Acad. Sci. USA. 89:1992;7305-7309.
76. Yamazaki T., Selkoe D.J., Koo E.H. Trafficking of cell surface β-amyloid precursor protein: Retrograde and transcytotic transport in cultured neurons. J. Cell Biol. 129:1995;431-442.
77. Yamazaki T., Koo E.H., Selkoe D.J. Cell surface amyloid β-protein precursor colocalizes with β-1 integrin at substrate contact sites in neural cells. J. Neurosci. 17:1997;1004-1010.
78. Yip J.W., Yip Y.P.L. Laminin-developmental expression and role in axonal outgrowth in the peripheral nervous system of the chick. Dev. Brain Res. 68:1995;23-33.