The Drosophila β-amyloid precursor protein homolog promotes synapse differentiation at the neuromuscular junction

Journal of Neuroscience

Volumn 19, Issue 18, 1999, Pages 7793-7803

  Torroja, Laura ^a   Packard, Mary ^b   Gorczyca, Michael ^b   White, Kalpana ^a   Budnik, Vivian ^b  

^a BRANDEIS UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Activity dependent synapse formation; Alzheimer's disease; APP; APPL; G(o) protein; Internalization; UAS Gal4

Indexed keywords

AMYLOID BETA PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN PRECURSOR;

ALZHEIMER DISEASE; ARTICLE; DROSOPHILA; GENE DELETION; GENE OVEREXPRESSION; IMMUNOCYTOCHEMISTRY; INTERNALIZATION; MOTONEURON; MUTANT; NEUROMUSCULAR JUNCTION DISORDER; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROCESSING; SEQUENCE HOMOLOGY; SYNAPTOGENESIS; TRANSMISSION ELECTRON MICROSCOPY;

DROSOPHILA;

EID: 0033568874     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-18-07793.1999     Document Type: Article

References (69)

1. Allinquant B, Moya K, Bouillot C, Prochiantz A (1994) Amyloid precursor protein in cortical neurons: coexistence of two pools differentially distributed in axons and dendrites and association with cytoskeleton. J Neurosci 14:6842-6854.
2. Atwood HL, Govind CK, Wu C-F (1993) Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J Neurobiol 24:1008-1024.
3. Bailey CH, Kandel ER (1993) Structural changes accompanying memory storage. Annu Rev Physiol 55:397-426.
4. Borg JP, Yang Y, De Taddeo-Borg M, Margolis B, and Turner RS (1998a) The X1 lalpha protein slows cellular amyloid precursor protein processing and reduces Aβ40 and Aβ42 secretion. J Biol Chem 273:14761-14766.
5. Borg JP, Straight SW, Kaech SM, de Taddeo-Borg M, Kroon DE, Karnak D, Turner RS, Kim SK, Margolis B (1998b) Identification of an evolutionarily conserved heterotrimeric protein complex involved in protein targeting. J Biol Chem 273:31633-31636.
6. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
7. o heterotrimeric protein within a cell compartment specialized in signal transduction. J Neurosci 19:1717-1727.
8. Budnik V, Zhong Y, Wu C-F (1990) Morphological plasticity of motor axon terminals in Drosophila mutants with altered excitability. J Neurosci 10:3754-3768.
9. Budnik V, Koh Y-H, Guan B, Hartmann B, Haugh C, Woods D, Gorczyca M (1996) Regulation of synapse structure and function by the Drosophila tumor suppressor gene, dlg. Neuron 17:627-640.
10. Buxbaum JD, Gandy SE, Cicchetti P, Ehrlich ME, Czernik AJ, Fracasso RP, Ramabhadran TV, Unterbeck AJ, Greengard P (1990) Processing of Alzheimer βA4 amyloid precursor protein: modulation by agents that regulates protein phosphorylation. Proc Natl Acad Sci USA 87:6003-6006.
11. Cline HT (1991) Activity-dependent plasticity in the visual systems of frogs and fish. Trends Neurosci 14:104-111.
12. Copenhaver PF, Horgan AM, Nichols DC, Rasmussen MA (1995) Developmental expression of heterotrimeric G proteins in the nervous system of Manduca sexta. J Neurobiol 26:461-484.
13. Daigle I, Li C (1993) apl-1, a Caenorhabditis elegans gene encoding a protein related to the human β-amyloid protein precursor. Proc Natl Acad Sci USA 90:12045-12049.
14. o α-like protein gene produces multiple transcripts and is expressed in the nervous system and ovaries. J Biol Chem 264:18544-18551.
15. Ermekova KS, Zambrano N, Linn H, Minopoli G, Gertler F, Russo T, Sudol M (1997) The WW domain of neural protein FE65 interacts with proline-rich motifs in Mena, the mammalian homolog of Drosophila enabled. J Biol Chem 272:32869-32877.
16. Furukawa K, Mattson MP (1998) Secreted amyloid precursor protein alpha selectively suppresses N-methyl-D-aspartate currents in hippocampal neurons: involvement of cyclic GMP. Neuroscience 83:429-438.
17. + channels and suppression of neuronal activity by secreted β-amyloid precursor protein. Nature 379:74-78.
18. Gandy S, Greengard P (1994) Regulated cleavage of the Alzheimer amyloid precursor protein: molecular and cellular basis. Biochimie 76:300-303.
19. Goh JW, Pennefather PS (1989) A pertussis toxin-sensitive G protein in hippocampus long-term potentiation. Science 244:980-983.
20. Gorczyca MG, Augart C, Budnik V (1993) Insulin-like receptor and insulin-like peptide are localized at neuromuscular junctions in Drosophila. J Neurosci 13:3692-3704.
21. Guan B, Hartmann B, Koh Y-H, Gorczyca M, Budnik V (1996) The Drosophila tumor suppressor gene, dlg, is involved in structural plasticity at a glutamatergic synapse. Curr Biol 6:695-706.
22. Hannan F, Zhong Y (1999) Second messenger systems underlying plasticity at the neuromuscular junction. In: Neuromuscular junctions in Drosophila: international review of neurobiology, Vol 43 (Budnik V, Gramates LS, eds), pp 119-138. San Diego: Academic.
23. Higgins LS, Catalano R, Quon D, Cordell B (1993) Transgenic mice expressing human β-APP751, but not mice expressing β-APP695, display early Alzheimer's disease-like histopathology. Ann NY Acad Sci 695:224-227.
24. Ishida A, Furukawa K, Keller JN, Mattson MP (1997) Secreted form of β-amyloid precursor protein shifts the frequency dependency for induction of LTD, and enhances LTP in hippocampal slices. NeuroReport 8:2133-2137.
25. Jia X, Gorczyca M, Budnik V (1993) Ultrastructure of neuromuscular junctions in Drosophila: comparison of wild type and mutants with increased excitability. J Neurobiol 24:1025-1044.
26. Kang J, Lemaire HG, Unterbeck A, Salbaum JM, Masters CL, Greschik KH, Multhaun G, Beyreuther K, Muller-Hill B (1987) The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325:733-736.
27. Klagges BR, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E (1996) Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154-3165.
28. Koo EH, Park L, Selkoe DJ (1993) Amyloid β-protein as a substrate interacts with extracellular matrix to promote neurite outgrowth. Proc Natl Acad Sci 90:4748-4752.
29. Koo EH, Squazzo SL, Selkoe DJ, Koo CH (1996) Trafficking of cell-surface amyloid β-protein precursor. I. Secretion, endocytosis and recycling as detected by labeled monoclonal antibody. J Cell Sci 109:991-998.
30. Kurdyak P, Atwood HL, Stewart BA, Wu CF (1994) Differential physiology and morphology of motor axons to ventral longitudinal muscles in larval Drosophila. J Comp Neurol 350:463-472.
31. Lahey T, Gorczyca M, Jia X, Budnik V (1994) The Drosophila tumor suppressor gene dig is required for normal synaptic bouton structure. Neuron 13:823-835.
32. Lai A, Sisodia SS, Trowbridge IS (1995) Characterization of sorting signals in the β-amyloid precursor protein cytoplasmic domain. J Biol Chem 270:3565-3573.
33. Lin DM, Goodman CS (1994) Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 13:507-523.
34. Littleton JT, Bellen HJ, Perin MS (1993) Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse. Development 118:1077-1088.
35. Loffler J, Huber G (1992) β-amyloid precursor protein isoforms in various rat brain regions and during brain development. J Neurochem 59:1316-1324.
36. Luo L (1992) Functional analysis of APPL, the Drosophila homologue of human amyloid precursor protein associated with Alzheimer's disease. PhD thesis, Brandeis University.
37. Luo L, Martin-Morris LE, White K (1990) Identification, secretion, and neural expression of APPL, a Drosophila protein similar to human amyloid protein precursor. J Neurosci 10:3849-3861.
38. Luo L, Tully T, White K (1992) Human amyloid precursor protein ameliorates behavioral deficit of flies deleted for Appl gene. Neuron 9:595-605.
39. Masliah E, Mallory M, Alford N, Mucke L (1995) Abnormal synaptic regeneration in hAPP695 transgenic and ApoE knockout mice. In: Research advances in Alzheimer's disease and related disorders (Iqbal K, Mortimer J, Winblad B, Wisniewsky H, eds), pp 405-414. New York: Wiley.
40. Mattson MP (1994) Secreted forms of β-amyloid precursor protein modulate dendrite outgrowth and calcium responses to glutamate in cultured embryonic hippocampal neurons. J Neurobiol 25:439-450.
41. Mattson MP (1997) Cellular actions of β-amyloid precursor protein and its soluble and fibrillogenic derivatives. Physiol Rev 77:1081-1132.
42. Moya KL, Benowitz LI, Schneider E, Allinquant B (1994) The amyloid precursor protein is developmentally regulated and correlated with synaptogenesis. Dev Biol 161:597-603.
43. Mucke L, Maslaih E, Johnson WB, Ruppe MD, Alford M, Rockenstein EM, Forss-Petter S, Pietropaolo M, Mallory M, Abraham CR (1994) Synaptotrophic effects of human amyloid β protein precursors in the cortex of transgenic mice. Brain Res 666:151-167.
44. Müller U, Cristina N, Li ZW, Wolfer DP, Lipp HP, Rulicke T, Brandner S, Aguzzi A, Weissmann C (1994) Behavioral and anatomical deficits in mice homozygous for a modified β-amyloid precursor protein gene. Cell 79:755-765.
45. o. Nature 362:75-79.
46. Nitsch RM, Slack BE, Farber SA, Schulz JG, Deng M, Kim C, Borghesani PR, Korver W, Wurtman RJ, Growdon JH (1994) Regulation of proteolytic processing of the amyloid β-protein precursor of Alzheimer's disease in transfected cell lines and in brain slices. J Neural Transm Suppl 44:21-27.
47. Okado H, Okamoto H (1992) A Xenopus homologue of the human beta-amyloid precursor protein: developmental regulation of its gene expression. Biochem Biophys Res Commun 189:1561-1568.
48. Okamoto T, Takeda S, Murayama Y, Ogata E, Nishimoto I (1995) Ligand-dependent G protein coupling function of amyloid transmembrane precursor. J Biol Chem 270:4205-4208.
49. Roch JM, Masliah E, Roch-Levecq AC, Sundsmo MP, Otero DA, Veinbergs I, Saitoh T (1994) Increase of synaptic density and memory retention by a peptide representing the trophic domain of the amyloid β/A4 protein precursor. Proc Natl Acad Sci USA 91:7450-7454.
50. Rosen DR, Martin-Morris L, Luo L, White K (1989) A Drosophila gene encoding a protein resembling the human β-amyloid protein precursor. Proc Natl Acad Sci USA 86:2478-2482.
51. Sastre M, Turner RS, Levy E (1998) X11 interaction with β-amyloid precursor protein modulates its cellular stabilization and reduces amyloid β-protein secretion. J Biol Chem 273:22351-22357.
52. Schuster CM, Davis GW, Fetter RD, Goodman CS (1996) Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron 17:641-654.
53. Sisodia SS (1994) Cellular and molecular genetic approaches in Alzheimer's disease. Neurobiol Aging [Suppl] 2:S135-S137.
54. Slunt HH, Thinakaran G, Koch CV, Lo AC, Tanzi RE, Sisodia SS (1994) Expression of a ubiquitous, cross-reactive homologue of the mouse β-amyloid precursor protein (APP). J Biol Chem 269:2637-2644.
55. Small DH (1998) The role of the amyloid protein precursor (APP) in Alzheimer's disease: does the normal function of APP explain the topography of neurodegeneration? Neurochem Res 23:795-806.
56. Small DH, Nurcombe V, Reed G, Clarris H, Beyreuther K, Masters CL (1994) The role of the extracellular matrix in regulating the function of the amyloid protein precursor of Alzheimer's disease. In: Amyloid protein precursor in development, aging and Alzheimer's disease (Masters CL, Beyreuther K, Trillet M, Christen Y, eds), pp 65-75. Berlin: Springer.
57. Spradling AC, Rubin GM (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218:341-347.
58. Strittmatter SM, Fishman MC, Zhu XP (1994) Activated mutants of the α subunit of G(o) promote an increased number of neurites per cell. J Neurosci 14:2327-2338.
59. Torroja L, Luo L, White K (1996) APPL, the Drosophila member of the APP-family, exhibits differential trafficking and processing in CNS neurons. J Neurosci 16:4638-4650.
60. Torroja L, Chu H, Kotovsky I, White K (1999) Neuronal overexpression of APPL, the Drosophila homologue of the amyloid precursor protein (APP), disrupts axonal transport. Curr Biol 9:489-492.
61. Trommsdorff M, Borg JP, Margolis B, Herz J (1998) Interaction of cytosolic adaptor proteins with neuronal apolipoprotein E receptors and the amyloid precursor protein. J Biol Chem 273:33556-33560.
62. Wasco W, Bupp K, Magendantz M, Gusella JF, Tanzi RE, Solomon F (1992) Identification of a mouse brain cDNA that encodes a protein related to the Alzheimer's disease-associated amyloid β protein precursor. Proc Natl Acad Sci USA 89:10758-10762.
63. Wasco W, Gurubhagavatula S, Paradis MD, Romano DM, Sisodia SS, Hyman BT, Neve RL, Tanzi RE (1993) Isolation and characterization of APLP2 encoding a homologue of the Alzheimer's associated amyloid β protein precursor. Nat Genet 5:95-100.
64. Weidemann A, Konig G, Bunke D, Fischer P, Salbaum JM, Masters CL, Beyreuther K (1989) Identification, biogenesis, and localization of precursors of Alzheimer's disease A4 amyloid protein. Cell 57:115-126.
65. Wolfgang WJ, Quan F, Goldsmith P, Unson C, Spiegel A, Forte M (1991) Restricted spatial and temporal expression of G protein α subunits during Drosophila embryogenesis. Development 113:527-538.
66. Woods DF, Bryant PJ (1991) The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66:451-464.
67. Zheng H, Jiang M, Trumbauer ME, Sirinathsinghji DJ, Hopkins R, Smith DW, Heavens RP, Dawson GR, Boyce S, Conner MW, Stevens KA, Slunt HH, Sisodia SS, Chen HY, Van der Ploeg LHT (1995) β-amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell 81:525-531.
68. Zinsmaier KE, Hofbauer A, Heimbeck G, Pflugfelder GO, Buchner S, Buchner E (1990) A cysteine-string protein is expressed in retina and brain of Drosophila. J Neurogenet 7:15-29.
69. Zito K, Parnas D, Fetter RD, Isacoff EY, Goodman CS (1999) Watching a synapse grow: noninvasive confocal imaging of synaptic growth in Drosophila. Neuron 22:719-729.