Amyloid precursor protein cytoplasmic domain antagonizes reelin neurite outgrowth inhibition of hippocampal neurons

Neurobiology of Aging

Volumn 29, Issue 4, 2008, Pages 542-553

  Hoareau, C ^a   Borrell, V ^b   Soriano, E ^b   Krebs, M O ^a   Prochiantz, A ^c   Allinquant, B ^a,c  

^a CENTRE PAUL BROCA   (France)

^b UNIVERSITY OF BARCELONA   (Spain)

^c ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

Alzheimer; Amyloid precursor protein; Disabled 1; Neurite outgrowth; Neuron; Reelin

Indexed keywords

AMYLOID PRECURSOR PROTEIN; REELIN; TYROSINE;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BIOTINYLATION; BRAIN NERVE CELL; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOPRECIPITATION; MOUSE; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

AMINO ACID SEQUENCE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOPLASM; EXTRACELLULAR MATRIX PROTEINS; HIPPOCAMPUS; MICE; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURAL INHIBITION; NEURITES; NEURONS; PROTEIN STRUCTURE, TERTIARY; RATS; SERINE ENDOPEPTIDASES;

EID: 39749154803     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2006.11.012     Document Type: Article

References (47)

1. Alcantara S., Ruiz M., D'Arcangelo G., Ezan F., de Lecea L., Curran T., et al. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J. Neurosci. 18 19 (1998) 7779-7799
2. Arnaud L., Ballif B.A., and Cooper J.A. Regulation of protein tyrosine kinase signaling by substrate degradation during brain development. Mol. Cell Biol. 23 24 (2003) 9293-9302
3. Beffert U., Weeber E.J., Durudas A., Qiu S., Masiulis I., Sweatt J.D., et al. Modulation of synaptic plasticity and memory by reelin involves differential splicing of the lipoprotein receptor Apoer2. Neuron 47 4 (2005) 567-579
4. Bertrand E., Brouillet E., Caille I., Bouillot C., Cole G.M., Prochiantz A., et al. A short cytoplasmic domain of the amyloid precursor protein induces apoptosis in vitro and in vivo. Mol. Cell. Neurosci. 18 5 (2001) 503-511
5. Borrell V., Ruiz M., Del Rio J.A., and Soriano E. Development of commissural connections in the hippocampus of reeler mice: evidence of an inhibitory influence of Cajal-Retzius cells. Exp. Neurol. 156 2 (1999) 268-282
6. Botella-Lopez A., Burgaya F., Gavin R., Garcia-Ayllon M.S., Gomez-Tortosa E., Pena-Casanova J., et al. Reelin expression and glycosylation patterns are altered in Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 103 14 (2006) 5573-5578
7. Brouillet E., Trembleau A., Galanaud D., Volovitch M., Bouillot C., Valenza C., et al. The amyloid precursor protein interacts with Go heterotrimeric protein within a cell compartment specialized in signal transduction. J. Neurosci. 19 5 (1999) 1717-1727
8. Cao X., and Sudhof T.C. A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293 5527 (2001) 115-120
9. Chen Y., Beffert U., Ertunc M., Tang T.S., Kavalali E.T., Bezprozvanny I., et al. Reelin modulates NMDA receptor activity in cortical neurons. J. Neurosci. 25 36 (2005) 8209-8216
10. D'Arcangelo G., and Curran T. Reeler: new tales on an old mutant mouse. Bioessays 20 3 (1998) 235-244
11. D'Arcangelo G., Homayouni R., Keshvara L., Rice D.S., Sheldon M., and Curran T. Reelin is a ligand for lipoprotein receptors. Neuron 24 2 (1999) 471-479
12. De Strooper B., and Annaert W. Proteolytic processing and cell biological functions of the amyloid precursor protein. J. Cell. Sci. 113 Pt 11 (2000) 1857-1870
13. Del Rio J.A., Heimrich B., Borrell V., Forster E., Drakew A., Alcantara S., et al. A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385 6611 (1997) 70-74
14. Derossi D., Chassaing G., and Prochiantz A. Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol. 8 2 (1998) 84-87
15. Hashimoto Y., Chiba T., Yamada M., Nawa M., Kanekura K., Suzuki H., et al. Transforming growth factor beta2 is a neuronal death-inducing ligand for amyloid-beta precursor protein. Mol. Cell Biol. 25 21 (2005) 9304-9317
16. Herms J., Anliker B., Heber S., Ring S., Fuhrmann M., Kretzschmar H., et al. Cortical dysplasia resembling human type 2 lissencephaly in mice lacking all three APP family members. EMBO J. 23 20 (2004) 4106-4115
17. Hiesberger T., Trommsdorff M., Howell B.W., Goffinet A., Mumby M.C., Cooper J.A., et al. Direct binding of reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24 2 (1999) 481-489
18. Hoe H.S., Magill L.A., Guenette S., Fu Z., Vicini S., and Rebeck G.W. FE65 Interaction with the apoE receptor ApoEr2. J. Biol. Chem. 281 34 (2006) 24521-24530
19. Homayouni R., Rice D.S., Sheldon M., and Curran T. Disabled-1 binds to the cytoplasmic domain of amyloid precursor-like protein 1. J. Neurosci. 19 17 (1999) 7507-7515
20. Hopker V.H., Shewan D., Tessier-Lavigne M., Poo M., and Holt C. Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401 6748 (1999) 69-73
21. Howell B.W., Lanier L.M., Frank R., Gertler F.B., and Cooper J.A. The disabled 1 phosphotyrosine-binding domain binds to the internalization signals of transmembrane glycoproteins and to phospholipids. Mol. Cell Biol. 19 7 (1999) 5179-5188
22. Joliot A., and Prochiantz A. Transduction peptides: from technology to physiology. Nat. Cell Biol. 6 3 (2004) 189-196
23. Kinoshita A., Whelan C.M., Smith C.J., Mikhailenko I., Rebeck G.W., Strickland D.K., et al. Demonstration by fluorescence resonance energy transfer of two sites of interaction between the low-density lipoprotein receptor-related protein and the amyloid precursor protein: role of the intracellular adapter protein Fe65. J. Neurosci. 21 21 (2001) 8354-8361
24. Langui D., Girardot N., El Hachimi K.H., Allinquant B., Blanchard V., Pradier L., et al. Subcellular topography of neuronal Abeta peptide in APPxPS1 transgenic mice. Am. J. Pathol. 165 5 (2004) 1465-1477
25. Lu D.C., Rabizadeh S., Chandra S., Shayya R.F., Ellerby L.M., Ye X., et al. A second cytotoxic proteolytic peptide derived from amyloid beta-protein precursor. Nat. Med. 6 4 (2000) 397-404
26. Madeira A., Pommet J.M., Prochiantz A., and Allinquant B. SET protein (TAF1beta, I2PP2A) is involved in neuronal apoptosis induced by an amyloid precursor protein cytoplasmic subdomain. FASEB J. 19 13 (2005) 1905-1907
27. Morimura T., Hattori M., Ogawa M., and Mikoshiba K. Disabled1 regulates the intracellular trafficking of reelin receptors. J. Biol. Chem. 280 17 (2005) 16901-16908
28. Niu S., Renfro A., Quattrocchi C.C., Sheldon M., and D'Arcangelo G. Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron 41 1 (2004) 71-84
29. Ogawa M., Miyata T., Nakajima K., Yagyu K., Seike M., Ikenaka K., et al. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14 5 (1995) 899-912
30. Ohkubo N., Lee Y.D., Morishima A., Terashima T., Kikkawa S., Tohyama M., et al. Apolipoprotein E and reelin ligands modulate tau phosphorylation through an apolipoprotein E receptor/disabled-1/glycogen synthase kinase-3beta cascade. FASEB J. 17 2 (2003) 295-297
31. Parisiadou L., and Efthimiopoulos S. Expression of mDab1 promotes the stability and processing of amyloid precursor protein and this effect is counteracted by X11alpha. Neurobiol. Aging (2006)
32. Passer B., Pellegrini L., Russo C., Siegel R.M., Lenardo M.J., Schettini G., et al. Generation of an apoptotic intracellular peptide by gamma-secretase cleavage of Alzheimer's amyloid beta protein precursor. J. Alzheimers Dis. 2 3-4 (2000) 289-301
33. Pietrzik C.U., Yoon I.S., Jaeger S., Busse T., Weggen S., and Koo E.H. FE65 constitutes the functional link between the low-density lipoprotein receptor-related protein and the amyloid precursor protein. J. Neurosci. 24 17 (2004) 4259-4265
34. Rohn T.T., Ivins K.J., Bahr B.A., Cotman C.W., and Cribbs D.H. A monoclonal antibody to amyloid precursor protein induces neuronal apoptosis. J. Neurochem. 74 6 (2000) 2331-2342
35. Rovelet-Lecrux A., Hannequin D., Raux G., Le Meur N., Laquerriere A., Vital A., et al. APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat. Genet. 38 1 (2006) 24-26
36. Selkoe D.J. Translating cell biology into therapeutic advances in Alzheimer's disease. Nature 399 Suppl. 6738 (1999) A23-A31
37. Sheldon M., Rice D.S., D'Arcangelo G., Yoneshima H., Nakajima K., Mikoshiba K., et al. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389 6652 (1997) 730-733
38. Stockinger W., Hengstschlager-Ottnad E., Novak S., Matus A., Huttinger M., Bauer J., et al. The low density lipoprotein receptor gene family. Differential expression of two alpha2-macroglobulin receptors in the brain. J. Biol. Chem. 273 48 (1998) 32213-32221
39. Strasser V., Fasching D., Hauser C., Mayer H., Bock H.H., Hiesberger T., et al. Receptor clustering is involved in reelin signaling. Mol. Cell Biol. 24 3 (2004) 1378-1386
40. Sudo H., Jiang H., Yasukawa T., Hashimoto Y., Niikura T., Kawasumi M., et al. Antibody-regulated neurotoxic function of cell-surface beta-amyloid precursor protein. Mol. Cell. Neurosci. 16 6 (2000) 708-723
41. Suh Y.H., and Checler F. Amyloid precursor protein, presenilins, and alpha-synuclein: molecular pathogenesis and pharmacological applications in Alzheimer's disease. Pharmacol. Rev. 54 3 (2002) 469-525
42. Tissir F., and Goffinet A.M. Reelin and brain development. Nat. Rev. Neurosci. 4 6 (2003) 496-505
43. Torroja L., Packard M., Gorczyca M., White K., and Budnik V. The Drosophila beta-amyloid precursor protein homolog promotes synapse differentiation at the neuromuscular junction. J. Neurosci. 19 18 (1999) 7793-7803
44. Trommsdorff M., Borg J.P., Margolis B., and Herz J. Interaction of cytosolic adaptor proteins with neuronal apolipoprotein E receptors and the amyloid precursor protein. J. Biol. Chem. 273 50 (1998) 33556-33560
45. Trommsdorff M., Gotthardt M., Hiesberger T., Shelton J., Stockinger W., Nimpf J., et al. Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97 6 (1999) 689-701
46. Weeber E.J., Beffert U., Jones C., Christian J.M., Forster E., Sweatt J.D., et al. Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J. Biol. Chem. 277 42 (2002) 39944-39952
47. Wirths O., Multhaup G., Czech C., Blanchard V., Tremp G., Pradier L., et al. Reelin in plaques of beta-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci. Lett. 316 3 (2001) 145-148