Amyloid precursor proteins interact with the heterotrimeric G protein go in the control of neuronal migration

Journal of Neuroscience

Volumn 33, Issue 24, 2013, Pages 10165-10181

  Ramaker, Jenna M ^a   Swanson, Tracy L ^a   Copenhaver, Philip F ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; ANTISENSE OLIGONUCLEOTIDE; GUANINE NUCLEOTIDE BINDING PROTEIN; MORPHOLINO OLIGONUCLEOTIDE; PROTEIN GO ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DROSOPHILA; EMBRYO; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MANDUCA; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; WESTERN BLOTTING;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BINDING SITES; BRAIN; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; COS CELLS; EMBRYO, NONMAMMALIAN; ENTERIC NERVOUS SYSTEM; FEMALE; GABA-A RECEPTOR ANTAGONISTS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HUMANS; IMMUNOPRECIPITATION; LUMINESCENT PROTEINS; MALE; MANDUCA; MICE; MORPHOLINOS; MUTATION; NEURONS; PICROTOXIN; PROTEIN BINDING; TRANSFECTION;

EID: 84878881555     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1146-13.2013     Document Type: Article

References (102)

1. Ashley J, Packard M, Ataman B, Budnik V (2005) Fasciclin II signals new synapse formation through amyloid precursor protein and the scaffolding protein dX11/Mint. J Neurosci 25:5943-5955.CrossRef Medline
2. Banker G, Goslin K (1998) Culturing nerve cells. Cambridge, MA: MIT. Bates CA,
3. Meyer RL (1996) Heterotrimeric G protein activation rapidly inhibits outgrowth of optic axons from adult and embryonic mouse, and goldfish retinal explants. Brain Res 714:65-75.CrossRef Medline
4. Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4:e20.CrossRef Medline
5. Bergmans BA, Shariati SA, Habets RL, Verstreken P, Schoonjans L, Müller U, Dotti CG, De Strooper B (2010) Neurons generated from APP/APLP1/ APLP2 triple knockout embryonic stem cells behave normally in vitro and in vivo: lack of evidence for a cell autonomous role of the amyloid precursor protein in neuronal differentiation. Stem Cells 28:399-406.Medline
6. Bolkan BJ, Triphan T, Kretzschmar D (2012) beta-secretase cleavage of the fly amyloid precursor protein is required for glial survival. J Neurosci 32:16181-16192.CrossRef Medline
7. Bourne HR, Sanders DA, McCormick F (1991) The GTPase superfamily: conserved structure and molecular mechanisms. Nature 349:117-127.CrossRef Medline
8. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.Medline
9. Bromberg KD, Iyengar R, He JC (2008) Regulation of neurite outgrowth by G(i/o) signaling pathways. Front Biosci 13:4544-4557.Medline
10. Brouillet E, Trembleau A, Galanaud D, Volovitch M, Bouillot C, Valenza C, Prochiantz A, Allinquant B (1999) The amyloid precursor protein interacts with Go heterotrimeric protein within a cell compartment specialized in signal transduction. J Neurosci 19:1717-1727.Medline
11. Carmine-Simmen K, Proctor T, Tschäpe J, Poeck B, Triphan T, Strauss R, Kretzschmar D (2009) Neurotoxic effects induced by the Drosophila amyloid-beta peptide suggest a conserved toxic function. Neurobiol Dis 33:274-281.CrossRef Medline
12. Chang KJ, Pugh W, Blanchard SG, McDermed J, Tam JP (1988) Antibody specific to the alpha subunit of the guanine nucleotide-binding regulatory protein Go: developmental appearance and immunocytochemical localization in brain. Proc Natl Acad Sci U S A 85:4929-4933.CrossRef Medline
13. Chen LT, Gilman AG, Kozasa T (1999) A candidate target for G protein action in brain. J Biol Chem 274:26931-26938.CrossRef Medline
14. Chen WJ, Goldstein JL, Brown MS (1990) NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J Biol Chem 265:3116-3123.Medline
15. Clarris HJ, Key B, Beyreuther K, Masters CL, Small DH (1995) Expression of the amyloid protein precursor of Alzheimer's disease in the developing rat olfactory system. Brain Res Dev Brain Res 88:87-95.CrossRef Medline
16. Coate TM, Swanson TL, Proctor TM, Nighorn AJ, Copenhaver PF (2007) Eph receptor expression defines midline boundaries for ephrin-positive migratory neurons in the enteric nervous system of Manduca sexta. J Comp Neurol 502:175-191.CrossRef Medline
17. Coate TM, Wirz JA, Copenhaver PF (2008) Reverse signaling via a glycosylphosphatidylinositol- linked ephrin prevents midline crossing by migratory neurons during embryonic development in Manduca. J Neurosci 28:3846-3860.CrossRef Medline
18. Coate TM, Swanson TL, Copenhaver PF (2009) Reverse signaling by GPIlinked Manduca Ephrin requires a src family kinase to restrict neuronal migration in vivo. J Neurosci 29:3404-3418.CrossRef Medline
19. Copenhaver PF, Taghert PH (1989a) Development of the enteric nervous system in the moth I. Diversity of cell types and the embryonic expression of FMRFamide-related neuropeptides. Dev Biol 131:70-84.CrossRef Medline
20. Copenhaver PF, Taghert PH (1989b) Development of the enteric nervous system in the moth II. Stereotyped cell migration precedes the differentiation of embryonic neurons. Dev Biol 131:85-101.CrossRef Medline
21. Copenhaver PF, Taghert PH (1990) Neurogenesis in the insect enteric nervous system: generation of pre-migratory neurons from an epithelial placode. Development 109:17-28.Medline
22. 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.CrossRef Medline
23. Copenhaver PF, Horgan AM, Combes S (1996) An identified set of visceral muscle bands is essential for the guidance of migratory neurons in the enteric nervous system of Manduca sexta. Dev Biol 179:412-426.CrossRef Medline
24. Dawson GR, Seabrook GR, Zheng H, Smith DW, Graham S, O'Dowd G, Bowery BJ, Boyce S, Trumbauer ME, Chen HY, Van der Ploeg LH, Sirinathsinghji DJ (1999) Age-related cognitive deficits, impaired long- term potentiation and reduction in synaptic marker density in mice lacking the beta-amyloid precursor protein. Neuroscience 90:1-13.CrossRef Medline
25. Devisme L, Bouchet C, Gonzalès M, Alanio E, Bazin A, Bessières B, Bigi N, Blanchet P, Bonneau D, Bonnières M, Bucourt M, Carles D, Clarisse B, Delahaye S, Fallet-Bianco C, Figarella-Branger D, Gaillard D, Gasser B, Delezoide AL, Guimiot F, et al. (2012) Cobblestone lissencephaly: neuropathological subtypes and correlations with genes of dystroglycanopathies. Brain 135:469-482.CrossRef Medline
26. Deyts C, Vetrivel KS, Das S, Shepherd YM, Dupré DJ, Thinakaran G, Parent AT (2012) Novel GαS-protein signaling associated with membranetethered amyloid precursor protein intracellular domain. J Neurosci 32: 1714-1729.CrossRef Medline
27. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454-1468.Medline
28. Dumanis SB, Chamberlain KA, Jin Sohn Y, Jin Lee Y, Guénette SY, Suzuki T, Mathews PM, Pak DTs, Rebeck GW, Suh YH, Park HS, Hoe HS (2012) FE65 as a link between VLDLR and APP to regulate their trafficking and processing. Mol Neurodegener 7:9.CrossRef Medline
29. Frémion F, Astier M, Zaffran S, Guillèn A, Homburger V, Sémériva M (1999) The heterotrimeric protein Go is required for the formation of heart epithelium in Drosophila. J Cell Biol 145:1063-1076.CrossRef Medline
30. Galés C, Van Durm JJ, Schaak S, Pontier S, Percherancier Y, Audet M, Paris H, Bouvier M (2006) Probing the activation-promoted structural rearrangements in preassembled receptor-G protein complexes. Nat Struct Mol Biol 13:778-786.CrossRef Medline
31. Gralle M, Ferreira ST (2007) Structure and functions of the human amyloid precursor protein: the whole is more than the sum of its parts. Prog Neurobiol 82:11-32.CrossRef Medline
32. Guénette S, Chang Y, Hiesberger T, Richardson JA, Eckman CB, Eckman EA, Hammer RE, Herz J (2006) Essential roles for the FE65 amyloid precursor protein-interacting proteins in brain development. EMBO J 25:420-431.CrossRef Medline
33. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-356.CrossRef Medline
34. Hartenstein V (1988) Development of Drosophila larval sensory organs: spatiotemporal pattern of sensory neurones, peripheral axonal pathways and sensilla differentiation. Development 102:869-886.
35. He JC, Neves SR, Jordan JD, Iyengar R (2006) Role of the Go/i signaling network in the regulation of neurite outgrowth. Can J Physiol Pharmacol 84:687-694.CrossRef Medline
36. Heber S, Herms J, Gajic V, Hainfellner J, Aguzzi A, Rülicke T, von Kretzschmar H, von Koch C, Sisodia S, Tremml P, Lipp HP, Wolfer DP, Müller U (2000) Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J Neurosci 20:7951-7963.Medline
37. Herms J, Anliker B, Heber S, Ring S, Fuhrmann M, Kretzschmar H, Sisodia S, Müller U (2004) Cortical dysplasia resembling human type 2 lissencephaly in mice lacking all three APP family members. EMBO J 23:4106-4115.CrossRef Medline
38. Higashijima T, Burnier J, Ross EM (1990) Regulation of Gi and Go by mastoparan, related amphiphilic peptides, and hydrophobic domains. J Biol Chem 265:14176-14186.Medline
39. Hiruma K, Riddiford LM (2004) Differential control of MHR3 promoter activity by isoforms of the ecdysone receptor and inhibitory effects of E75A and MHR3. Dev Biol 272:510-521.CrossRef Medline
40. Ho A, Südhof TC (2004) Binding of F-spondin to amyloid-beta precursor protein: a candidate amyloid-beta precursor protein ligand that modulates amyloid-beta precursor protein cleavage. Proc Natl Acad Sci U S A 101:2548-2553.CrossRef Medline
41. Hoe HS, Rebeck GW (2008) Functional interactions of APP with the apoE receptor family. J Neurochem 106:2263-2271.CrossRef Medline
42. Horgan AM, Copenhaver PF (1998) G protein-mediated inhibition of neuronal migration requires calcium influx. J Neurosci 18:4189-4200.Medline
43. Horgan AM, Lagrange MT, Copenhaver PF (1994) Developmental expression of G proteins in a migratory population of embryonic neurons. Development 120:729-742.Medline
44. α in a migratory population of embryonic neurons. Dev Biol 172:640-653.CrossRef Medline
45. Hortsch M (1994) Preparation and analysis of membranes and membrane proteins from Drosophila. Methods Cell Biol 44:289-301.CrossRef Medline
46. Igarashi M, Strittmatter SM, Vartanian T, Fishman MC (1993) Mediation by G proteins of signals that cause collapse of growth cones. Science 259:77-79.CrossRef Medline
47. Karran E, Mercken M, De Strooper B (2011) The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics. Nat Rev Drug Discov 10:698-712.CrossRef Medline
48. Kerppola TK (2008) Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Annual review of biophysics 37:465-487.CrossRef Medline
49. Khachaturian ZS (1987) Hypothesis on the regulation of cytosol calcium concentration and the aging brain. Neurobiol Aging 8:345-346.CrossRef Medline
50. LaFerla FM (2002) Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease. Nat Rev Neurosci 3:862-872.CrossRef Medline
51. Leyssen M, Ayaz D, Hébert SS, Reeve S, De Strooper B, Hassan BA (2005) Amyloid precursor protein promotes post-developmental neurite arborization in the Drosophila brain. EMBO J 24:2944-2955.CrossRef Medline
52. Luo LQ, 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.Medline
53. Luo L, Tully T, White K (1992) Human amyloid precursor protein ameliorates behavioral deficit of flies deleted for Appl gene. Neuron 9:595-605.CrossRef Medline
54. Mangialasche F, Solomon A, Winblad B, Mecocci P, Kivipelto M (2010) Alzheimer's disease: clinical trials and drug development. Lancet Neurol 9:702-716.CrossRef Medline
55. Mangmool S, Kurose H (2011) G(i/o) Protein-Dependent and -Independent Actions of Pertussis Toxin (PTX). Toxins 3:884-899.CrossRef Medline
56. Martin-Morris LE, White K (1990) The Drosophila transcript encoded by the beta-amyloid protein precursor-like gene is restricted to the nervous system. Development 110:185-195.Medline
57. McLoughlin DM, Miller CC (2008) The FE65 proteins and Alzheimer's disease. J Neurosci Res 86:744-754.CrossRef Medline
58. Mervine SM, Yost EA, Sabo JL, Hynes TR, Berlot CH (2006) Analysis of G protein betagamma dimer formation in live cells using multicolor bimolecular fluorescence complementation demonstrates preferences of beta1 for particular gamma subunits. Mol Pharmacol 70:194-205.Medline
59. Mora N, Almudi I, Alsina B, Corominas M, Serras F (2013) beta amyloid protein precursor-like (Appl) is a Ras1/MAPK-regulated gene required for axonal targeting in Drosophila photoreceptor neurons. J Cell Sci 126: 53-59.CrossRef Medline
60. Muresan V, Varvel NH, Lamb BT, Muresan Z (2009) The cleavage products of amyloid-beta precursor protein are sorted to distinct carrier vesicles that are independently transported within neurites. J Neurosci 29:3565-3578.CrossRef Medline
61. Nakayama T, Goshima Y, Misu Y, Kato T (1999) Role of cdk5 and tau phosphorylation in heterotrimeric G protein-mediated retinal growth cone collapse. J Neurobiol 41:326-339.CrossRef Medline
62. Nishimoto I, Okamoto T, Matsuura Y, Takahashi S, Okamoto T, Murayama Y, Ogata E (1993) Alzheimer amyloid protein precursor complexes with brain GTP-binding protein Go. Nature 362:75-79.CrossRef Medline
63. Okamoto T, Katada T, Murayama Y, Ui M, Ogata E, Nishimoto I (1990) A simple structure encodes G protein-activating function of the IGF-II/ mannose 6-phosphate receptor. Cell 62:709-717.CrossRef Medline
64. Okamoto T, Takeda S, Murayama Y, Ogata E, Nishimoto I (1995) Liganddependent G protein coupling function of amyloid transmembrane precursor. J Biol Chem 270:4205-4208.CrossRef Medline
65. Okamoto T, Takeda S, Giambarella U, Murayama Y, Matsui T, Katada T, Matsuura Y, Nishimoto I (1996) Intrinsic signaling function of APP as a novel target of three V642 mutations linked to familial Alzheimer's disease. EMBO J 15:3769-3777.Medline
66. Osterfield M, Egelund R, Young LM, Flanagan JG (2008) Interaction of amyloid precursor protein with contactins and NgCAM in the retinotectal system. Development 135:1189-1199.CrossRef Medline
67. Patel TB (2004) Single transmembrane spanning heterotrimeric G protein-coupled receptors and their signaling cascades. Pharmacol Rev 56:371-385.CrossRef Medline
68. Perez RG, Zheng H, Van der Ploeg LH, Koo EH (1997) The beta-amyloid precursor protein of Alzheimer's disease enhances neuron viability and modulates neuronal polarity. J Neurosci 17:9407-9414.Medline
69. Phinney AL, Calhoun ME, Wolfer DP, Lipp HP, Zheng H, Jucker M (1999) No hippocampal neuron or synaptic bouton loss in learningimpaired aged beta-amyloid precursor protein-null mice. Neuroscience 90:1207-1216.CrossRef Medline
70. Pramatarova A, Ochalski PG, Lee CH, Howell BW (2006) Mouse disabled 1 regulates the nuclear position of neurons in a Drosophila eye model. Mol Cell Biol 26:1510-1517.CrossRef Medline
71. Qiu WQ, Ferreira A, Miller C, Koo EH, Selkoe DJ (1995) Cell-surface betaamyloid precursor protein stimulates neurite outgrowth of hippocampal neurons in an isoform-dependent manner. J Neurosci 15:2157-2167.Medline
72. Reinhard C, Hébert SS, De Strooper B (2005) The amyloid-beta precursor protein: integrating structure with biological function. EMBO J 24:3996-4006.CrossRef Medline
73. Reis K, Zharkovsky A, Bogdanovic N, Karelson E, Land T (2007) Critical role of methionine-722 in the stimulation of human brain G-proteins and neurotoxicity induced by London familial Alzheimer's disease (FAD) mutated V717G-APP(714-723). Neuroscience 144:571-578.CrossRef Medline
74. Remy I, Montmarquette A, Michnick SW (2004) PKB/Akt modulates TGFbeta signalling through a direct interaction with Smad3. Nat Cell Biol 6:358-365.CrossRef Medline
75. Rice HC, Townsend M, Bai J, Suth S, Cavanaugh W, Selkoe DJ, Young-Pearse TL (2012) Pancortins interact with amyloid precursor protein and modulate cortical cell migration. Development 139:3986-3996.CrossRef Medline
76. Robida AM, Kerppola TK (2009) Bimolecular fluorescence complementation analysis of inducible protein interactions: effects of factors affecting protein folding on fluorescent protein fragment association. J Mol Biol 394:391-409.CrossRef Medline
77. Sabo SL, Ikin AF, Buxbaum JD, Greengard P (2003) The amyloid precursor protein and its regulatory protein, FE65, in growth cones and synapses in vitro and in vivo. J Neurosci 23:5407-5415.Medline
78. Shaked GM, Chauv S, Ubhi K, Hansen LA, Masliah E (2009) Interactions between the amyloid precursor protein C-terminal domain and G proteins mediate calcium dysregulation and amyloid beta toxicity in Alzheimer's disease. FEBS J 276:2736-2751.CrossRef Medline
79. Shariati SA, Lau P, Hassan BA, Müller U, Dotti CG, De Strooper B, Gärtner A (2013) APLP2 regulates neuronal stem cell differentiation during cortical development. J Cell Sci 126:1268-1277.CrossRef Medline
80. Soba P, Eggert S, Wagner K, Zentgraf H, Siehl K, Kreger S, Löwer A, Langer A, Merdes G, Paro R, Masters CL, Müller U, Kins S, Beyreuther K (2005) Homo- and heterodimerization of APP family members promotes intercellular adhesion. EMBO J 24:3624-3634.CrossRef Medline
81. Sola Vigo F, Kedikian G, Heredia L, Heredia F, Añel AD, Rosa AL, Lorenzo A (2009) Amyloid-beta precursor protein mediates neuronal toxicity of amyloid beta through Go protein activation. Neurobiol Aging 30: 1379-1392.CrossRef Medline
82. Sprecher SG, Cardona A, Hartenstein V (2011) The Drosophila larval visual system: high-resolution analysis of a simple visual neuropil. Dev Biol 358:33-43.CrossRef Medline
83. Steller H, Fischbach KF, Rubin GM (1987) Disconnected: a locus required for neuronal pathway formation in the visual system of Drosophila. Cell 50:1139-1153.CrossRef Medline
84. Sternweis PC, Gilman AG (1982) Aluminum: a requirement for activation of the regulatory component of adenylate cyclase by fluoride. Proc Natl Acad Sci U S A 79:4888-4891.CrossRef Medline
85. Strathmann M, Simon MI (1990) G protein diversity: a distinct class of α-subunits is present in vertebrates and invertebrates. Proc Natl Acad Sci U S A 87:9113-9117.CrossRef Medline
86. Strittmatter SM (1992) GAP-43 as a modulator ofGprotein transduction in the growth cone. Perspect Dev Neurobiol 1:13-19.Medline
87. Stryer L, Bourne HR (1986) Gproteins: a family of signal transducers. Annu Rev Cell Biol 2:391-419.CrossRef Medline
88. Sugaya K, Chouinard M, Greene R, Robbins M, Personett D, Kent C, Gallagher M, McKinney M (1996) Molecular indices of neuronal and glial plasticity in the hippocampal formation in a rodent model of age-induced spatial learning impairment. J Neurosci 16:3427-3443.Medline
89. Swanson TL, Knittel LM, Coate TM, Farley SM, Snyder MA, Copenhaver PF (2005) The insect homologue of the amyloid precursor protein interacts with the heterotrimeric G protein Go alpha in an identified population of migratory neurons. Dev Biol 288:160-178.CrossRef Medline
90. α-like proteins in the Drosophila CNS. J Biol Chem 264:18552-18560.Medline
91. Timossi C, Ortiz-Elizondo C, Pineda DB, Dias JA, Conn PM, Ulloa-Aguirre A (2004) Functional significance of the BBXXB motif reversed present in the cytoplasmic domains of the human follicle-stimulating hormone receptor. Mol Cell Endocrinol 223:17-26.CrossRef Medline
92. Tix S, Minden JS, Technau GM (1989) Pre-existing neuronal pathways in the developing optic lobes of Drosophila. Development 105:739-746.Medline
93. Torroja L, Chu H, Kotovsky I, White K (1999a) Neuronal overexpression of APPL, the Drosophila homologue of the amyloid precursor protein (APP), disrupts axonal transport. Curr Biol 9:489-492.CrossRef Medline
94. Torroja L, Packard M, Gorczyca M, White K, Budnik V (1999b) The Drosophila beta-amyloid precursor protein homolog promotes synapse differentiation at the neuromuscular junction. J Neurosci 19:7793-7803.Medline
95. Turner PR, O'Connor K, Tate WP, Abraham WC (2003) Roles of amyloid precursor protein and its fragments in regulating neural activity, plasticity and memory. Prog Neurobiol 70:1-32.CrossRef Medline
96. Wentzell JS, Bolkan BJ, Carmine-Simmen K, Swanson TL, Musashe DT, Kretzschmar D (2012) Amyloid precursor proteins are protective in Drosophila models of progressive neurodegeneration. Neurobiol Dis 46: 78-87.CrossRef Medline
97. Wright JW, Schwinof KM, Snyder MA, Copenhaver PF (1998) A delayed role for nitric oxide-sensitive guanylate cyclases in a migratory population of embryonic neurons. Dev Biol 203:15-33.
98. Wright JW, Snyder MA, Schwinof KM, Combes S, Copenhaver PF (1999) A role for fasciclin II in the guidance of neuronal migration. Development 126:3217-3228.Medline
99. Wu D, Jiang H, Simon MI (1995) Different alpha 1-adrenergic receptor sequences required for activating different G alpha subunits of Gq class of G proteins. J Biol Chem 270:9828-9832.CrossRef Medline
100. Yamatsuji T, Matsui T, Okamoto T, Komatsuzaki K, Takeda S, Fukumoto H, Iwatsubo T, Suzuki N, Asami-Odaka A, Ireland S, Kinane TB, Giambarella U, Nishimoto I (1996) G protein-mediated neuronal DNA fragmentation induced by familial Alzheimer's disease-associated mutants of APP. Science 272:1349-1352.CrossRef Medline
101. Young-Pearse TL, Bai J, Chang R, Zheng JB, LoTurco JJ, Selkoe DJ (2007) A critical function for beta-amyloid precursor protein in neuronal migration revealed by in utero RNA interference. J Neurosci 27:14459-14469.CrossRef Medline
102. Young-Pearse TL, Chen AC, Chang R, Marquez C, Selkoe DJ (2008) Secreted APP regulates the function of full-length APP in neurite outgrowth through interaction with integrin beta1. Neural Dev 3:15.CrossRef Medline