UV irradiation accelerates amyloid precursor protein (APP) processing and disrupts APP axonal transport

Journal of Neuroscience

Volumn 34, Issue 9, 2014, Pages 3320-3339

  Almenar Queralt, Angels ^a,e   Falzone, Tomas L ^a,g   Shen, Zhouxin ^d   Lillo, Concepcion ^c,f   Killian, Rhiannon L ^a   Arreola, Angela S ^a,e   Niederst, Emily D ^a   Ng, Kheng S ^a   Kim, Sonia N ^a,e   Briggs, Steven P ^d   Williams, David S ^c,h   Goldstein, Lawrence S B ^a,b,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e SANFORD CONSORTIUM FOR REGENERATIVE MEDICINE   (United States)

^f UNIVERSITY OF SALAMANCA   (Spain)

^g Facultad de Medicina   (Argentina)

^h JULES STEIN EYE INSTITUTE   (United States)

Author keywords

Amyloid precursor protein; APP axonal vesicles; Axonal transport; Gamma secretase; Kinesin; UV irradiation

Indexed keywords

2 CHLORO 3 (3,4 DICHLOROPHENYL) 1 ISOPROPYL 4 METHYLIMIDAZOLIUM CHLORIDE; AMMONIUM CHLORIDE; AMYLOID PRECURSOR PROTEIN; AMYLOID PRECURSOR PROTEIN LIKE PROTEIN 1; AMYLOID PRECURSOR PROTEIN LIKE PROTEIN 2; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BETA SECRETASE 1; CALNEXIN; CATHEPSIN D; CYCLOHEXIMIDE; DYNASORE; ENZYME INHIBITOR; GAMMA SECRETASE; GAMMA SECRETASE INHIBITOR; KINESIN 1; NEUROMODULIN; NICASTRIN; PEPTIDES AND PROTEINS; PRESENILIN 1; PROTEIN PEN2; RAB PROTEIN; STRESS ACTIVATED PROTEIN KINASE; SYNAPSIN I; SYNAPTOBREVIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; ELECTROKYMOGRAPHY; ELECTRON MICROSCOPY; FEMALE; GENE EXPRESSION; GENE ONTOLOGY; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MOUSE; NERVE FIBER TRANSPORT; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SYNAPTOSOME; ULTRAVIOLET IRRADIATION; WESTERN BLOTTING;

AMYLOID PRECURSOR PROTEIN; APP AXONAL VESICLES; AXONAL TRANSPORT; GAMMA-SECRETASE; KINESIN; UV-IRRADIATION;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; AXONAL TRANSPORT; AXONS; CELLS, CULTURED; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROBLASTOMA; NEURONS; PRESENILIN-1; PRESENILIN-2; TRANSFECTION; ULTRAVIOLET RAYS;

EID: 84894431292     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1503-13.2014     Document Type: Article

References (88)

1. Abe N, Almenar-Queralt A, Lillo C, Shen Z, Lozach J, Briggs SP, Williams DS, Goldstein LS, Cavalli V (2009) Sunday driver interacts with two distinct classes of axonal organelles. J Biol Chem 284:34628-34639. CrossRef Medline
2. Amaratunga A, Fine RE (1995) Generation of amyloidogenic C-terminal fragments during rapid axonal transport in vivo of beta-amyloid precursor protein in the optic nerve. J Biol Chem 270:17268-17272. CrossRef Medline
3. Amaratunga A, Leeman SE, Kosik KS, Fine RE (1995) Inhibition of kinesin synthesis in vivo inhibits the rapid transport of representative proteins for three transport vesicle classes into the axon. J Neurochem 64:2374-2376. Medline
4. Araki Y, Tomita S, Yamaguchi H, Miyagi N, Sumioka A, Kirino Y, Suzuki T (2003) Novel cadherin-related membrane proteins, Alcadeins, enhance the X11-like protein-mediated stabilization of amyloid beta-protein precursor metabolism. J Biol Chem 278:49448-49458. CrossRef Medline
5. Araki Y, Kawano T, Taru H, Saito Y, Wada S, Miyamoto K, Kobayashi H, Ishikawa HO, Ohsugi Y, Yamamoto T, Matsuno K, Kinjo M, Suzuki T (2007) The novel cargo Alcadein induces vesicle association of kinesin-1 motor components and activates axonal transport. EMBO J 26:1475-1486. CrossRef Medline
6. Beher D, Elle C, Underwood J, Davis JB, Ward R, Karran E, Masters CL, Beyreuther K, Multhaup G (1999) Proteolytic fragments of Alzheimer's disease-associated presenilin 1 are present in synaptic organelles and growth cone membranes of rat brain. J Neurochem 72:1564-1573. Medline
7. Brunholz S, Sisodia S, Lorenzo A, Deyts C, Kins S, Morfini G (2012) Axonal transport of APP and the spatial regulation of APP cleavage and function in neuronal cells. Exp Brain Res 217:353-364. CrossRef Medline
8. Caporaso GL, Takei K, Gandy SE, Matteoli M, Mundigl O, Greengard P, De Camilli P (1994) Morphologic and biochemical analysis of the intracellular trafficking of the Alzheimer beta/A4 amyloid precursor protein. J Neurosci 14:3122-3138. Medline
9. Carey RM, Balcz BA, Lopez-Coviella I, Slack BE (2005) Inhibition of dynamin-dependent endocytosis increases shedding of the amyloid precursor protein ectodomain and reduces generation of amyloid beta protein. BMC Cell Biol 6:30. CrossRef Medline
10. Cavalli V, Vilbois F, Corti M, Marcote MJ, Tamura K, Karin M, Arkinstall S, Gruenberg J (2001) The stress-inducedMAPkinase p38 regulates endocytic trafficking via the GDI:Rab5 complex. Mol Cell 7:421-432. CrossRef Medline
11. Chen XH, Siman R, Iwata A, Meaney DF, Trojanowski JQ, SmithDH (2004) Long-term accumulation of amyloid-beta, beta-secretase, presenilin-1, and caspase-3 in damaged axons following brain trauma. Am J Pathol 165:357-371. CrossRef Medline
12. Cirrito JR, Kang JE, Lee J, Stewart FR, Verges DK, Silverio LM, Bu G, Mennerick S, Holtzman DM (2008) Endocytosis is required for synaptic activity-dependent release of amyloid-beta in vivo. Neuron 58:42-51. CrossRef Medline
13. Cole GM, Huynh TV, Saitoh T (1989) Evidence for lysosomal processing of amyloid beta-protein precursor in cultured cells. Neurochem Res 14:933-939. CrossRef Medline
14. Corrigan F, Vink R, Blumbergs PC, Masters CL, Cappai R, van den Heuvel C (2012) Characterisation of the effect of knockout of the amyloid precursor protein on outcome following mild traumatic brain injury. Brain Res 1451:87-99. CrossRef Medline
15. Cuesta A, Zambrano A, López E, Pascual A (2009a) Thyroid hormones reverse the UV-induced repression of APP in neuroblastoma cells. FEBS Lett 583:2401-2406. CrossRef Medline
16. Cuesta A, Zambrano A, Royo M, Pascual A (2009b) The tumour suppressor p53 regulates the expression of amyloid precursor protein (APP). Biochem J 418:643-650. CrossRef Medline
17. Falzone TL, Stokin GB (2012) Imaging amyloid precursor protein in vivo: an axonal transport assay. Methods Mol Biol 846:295-303. CrossRef Medline
18. Falzone TL, Stokin GB, Lillo C, Rodrigues EM, Westerman EL, Williams DS, Goldstein LS (2009) Axonal stress kinase activation and tau misbehavior induced by kinesin-1 transport defects. J Neurosci 29:5758-5767. CrossRef Medline
19. Frykman S, Hur JY, Frånberg J, Aoki M, Winblad B, Nahalkova J, Behbahani H, Tjernberg LO (2010) Synaptic and endosomal localization of active gamma-secretase in rat brain. PLoS One 5:e8948. CrossRef Medline
20. Fu MM, Holzbaur EL (2013) JIP1 regulates the directionality of APP axonal transport by coordinating kinesin and dynein motors. J Cell Biol 202:495-508. CrossRef Medline
21. Golde TE, Estus S, Younkin LH, Selkoe DJ, Younkin SG (1992) Processing of the amyloid protein precursor to potentially amyloidogenic derivatives. Science 255:728-730. CrossRef Medline
22. Goldsbury C, Mocanu MM, Thies E, Kaether C, Haass C, Keller P, Biernat J, Mandelkow E, Mandelkow EM (2006) Inhibition of APP trafficking by tau protein does not increase the generation of amyloid-beta peptides. Traffic 7:873-888. CrossRef Medline
23. Goldstein LS (2012) Axonal transport and neurodegenerative disease: can we see the elephant? Prog Neurobiol 99:186-190. CrossRef Medline
24. Groemer TW, Thiel CS, Holt M, Riedel D, Hua Y, Hüve J, Wilhelm BG, Klingauf J (2011) Amyloid precursor protein is trafficked and secreted via synaptic vesicles. PLoS One 6:e18754. CrossRef Medline
25. Gunawardena S, Goldstein LS (2001) Disruption of axonal transport and neuronal viability by amyloid precursor protein mutations in Drosophila. Neuron 32:389-401. CrossRef Medline
26. Haapasalo A, Kovacs DM (2011) The many substrates of presenilin/γ-secretase. J Alzheimers Dis 25:3-28. CrossRef Medline
27. Hata S, Fujishige S, Araki Y, Kato N, Araseki M, Nishimura M, Hartmann D, Saftig P, Fahrenholz F, Taniguchi M, Urakami K, Akatsu H, Martins RN, Yamamoto K, Maeda M, Yamamoto T, Nakaya T, Gandy S, Suzuki T (2009) Alcadein cleavages by amyloid beta-precursor protein (APP) alpha-and gamma-secretases generate small peptides, p3-Alcs, indicating Alzheimer disease-related gamma-secretase dysfunction. J Biol Chem 284:36024-36033. CrossRef Medline
28. Huttner WB, Schiebler W, Greengard P, De Camilli P (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol 96:1374-1388. CrossRef Medline
29. Ikin AF, Annaert WG, Takei K, De Camilli P, Jahn R, Greengard P, Buxbaum JD (1996) Alzheimer amyloid protein precursor is localized in nerve terminal preparations to Rab5-containing vesicular organelles distinct from those implicated in the synaptic vesicle pathway. J Biol Chem 271: 31783-31786. CrossRef Medline
30. Inomata H, Nakamura Y, Hayakawa A, Takata H, Suzuki T, Miyazawa K, Kitamura N (2003) A scaffold protein JIP-1b enhances amyloid precursor protein phosphorylation by JNK and its association with kinesin light chain 1. J Biol Chem 278:22946-22955. CrossRef Medline
31. Ip YT, Davis RJ (1998) Signal transduction by the c-Jun N-terminal kinase (JNK)-from inflammation to development. Curr Opin Cell Biol 10:205-219. CrossRef Medline
32. Israel MA, Yuan SH, Bardy C, Reyna SM, MuY, Herrera C, Hefferan MP, Van Gorp S, Nazor KL, Boscolo FS, Carson CT, Laurent LC, Marsala M, Gage FH, Remes AM, Koo EH, Goldstein LS (2012) Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 482:216-220. CrossRef Medline
33. Jin SM, Cho HJ, Jung MW, Mook-Jung I (2007) DNA damage-inducing agent-elicited gamma-secretase activity is dependent on Bax/Bcl-2 pathway but not on caspase cascades. Cell Death Differ 14:189-192. CrossRef Medline
34. Jin SM, Cho HJ, Jung ES, Shim MY, Mook-Jung I (2008) DNA damageinducing agents elicit gamma-secretase activation mediated by oxidative stress. Cell Death Differ 15:1375-1384. CrossRef Medline
35. Kaether C, Skehel P, Dotti CG (2000) Axonal membrane proteins are transported in distinct carriers: a two-color video microscopy study in cultured hippocampal neurons. Mol Biol Cell 11:1213-1224. CrossRef Medline
36. Kamal A, Stokin GB, Yang Z, Xia CH, Goldstein LS (2000) Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28:449-459. CrossRef Medline
37. Kamal A, Almenar-Queralt A, LeBlanc JF, Roberts EA, Goldstein LS (2001) Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 414:643-648. CrossRef Medline
38. Kang DE, Yoon IS, Repetto E, Busse T, Yermian N, Ie L, Koo EH (2005) Presenilins mediate phosphatidylinositol 3-kinase/AKT and ERK activation via select signaling receptors. Selectivity of PS2 in platelet-derived growth factor signaling. J Biol Chem 280:31537-31547. CrossRef Medline
39. Kasa P, Papp H, Pakaski M (2001) Presenilin-1 and its N-terminal and C-terminal fragments are transported in the sciatic nerve of rat. Brain Res 909:159-169. CrossRef Medline
40. Kohli BM, Pflieger D, Mueller LN, Carbonetti G, Aebersold R, Nitsch RM, Konietzko U (2012) Interactome of the amyloid precursor protein APP in brain reveals a protein network involved in synaptic vesicle turnover and a close association with Synaptotagmin-1. J Proteome Res 11:4075-4090. CrossRef Medline
41. Konecna A, Frischknecht R, Kinter J, Ludwig A, Steuble M, Meskenaite V, Indermühle M, Engel M, Cen C, Mateos JM, Streit P, Sonderegger P (2006) Calsyntenin-1 docks vesicular cargo to kinesin-1. Mol Biol Cell 17:3651-3663. CrossRef Medline
42. Koo EH, Squazzo SL (1994) Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J Biol Chem 269: 17386-17389. Medline
43. Lazarov O, Morfini GA, Lee EB, Farah MH, Szodorai A, DeBoer SR, Koliatsos VE, Kins S, Lee VM, Wong PC, Price DL, Brady ST, Sisodia SS (2005) Axonal transport, amyloid precursor protein, kinesin-1, and the processing apparatus: revisited. J Neurosci 25:2386-2395. CrossRef Medline
44. Lee PH, Hwang EM, Hong HS, Boo JH, Mook-Jung I, Huh K (2006) Effect of ischemic neuronal insults on amyloid precursor protein processing. Neurochem Res 31:821-827. CrossRef Medline
45. 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
46. Li L, Zhang X, Yang D, Luo G, Chen S, LeW (2009) Hypoxia increases Abeta generation by altering beta-and gamma-cleavage of APP. Neurobiol Aging 30:1091-1098. CrossRef Medline
47. Ludwig A, Blume J, Diep TM, Yuan J, Mateos JM, Leuthäuser K, Steuble M, Streit P, Sonderegger P (2009) Calsyntenins mediateTGNexit of APP in a kinesin-1-dependent manner. Traffic 10:572-589. CrossRef Medline
48. Lyckman AW, Confaloni AM, Thinakaran G, Sisodia SS, Moya KL (1998) Post-translational processing and turnover kinetics of presynaptically targeted amyloid precursor superfamily proteins in the central nervous system. J Biol Chem 273:11100-11106. CrossRef Medline
49. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10:839-850. CrossRef Medline
50. Marquez-Sterling NR, Lo AC, Sisodia SS, Koo EH (1997) Trafficking of cell-surface beta-amyloid precursor protein: evidence that a sorting intermediate participates in synaptic vesicle recycling. J Neurosci 17:140-151. Medline
51. Matsuda S, Matsuda Y, D'Adamio L (2003) Amyloid beta protein precursor (AbetaPP), but not AbetaPP-like protein 2, is bridged to the kinesin light chain by the scaffold protein JNK-interacting protein 1. J Biol Chem 278:38601-38606. CrossRef Medline
52. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G (2010) GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 28:495-501. CrossRef Medline
53. Minopoli G, Stante M, Napolitano F, Telese F, Aloia L, De Felice M, Di Lauro R, Pacelli R, Brunetti A, Zambrano N, Russo T (2007) Essential roles for Fe65, Alzheimer amyloid precursor-binding protein, in the cellular response to DNA damage. J Biol Chem 282:831-835. Medline
54. 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
55. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457:981-989. CrossRef Medline
56. Nunan J, Shearman MS, Checler F, Cappai R, Evin G, Beyreuther K, Masters CL, Small DH (2001) The C-terminal fragment of the Alzheimer's disease amyloid protein precursor is degraded by a proteasome-dependent mechanism distinct from gamma-secretase. Eur J Biochem 268:5329-5336. CrossRef Medline
57. Oksvold MP, Huitfeldt HS, Østvold AC, Skarpen E (2002) UV induces tyrosine kinase-independent internalisation and endosome arrest of the EGF receptor. J Cell Sci 115:793-803. Medline
58. Papp H, Pakaski M, Kasa P (2002) Presenilin-1 and the amyloid precursor protein are transported bidirectionally in the sciatic nerve of adult rat. Neurochem Int 41:429-435. CrossRef Medline
59. Reis GF, Yang G, Szpankowski L, Weaver C, Shah SB, Robinson JT, Hays TS, Danuser G, Goldstein LS (2012) Molecular motor function in axonal transport in vivo probed by genetic and computational analysis in Drosophila. Mol Biol Cell 23:1700-1714. CrossRef Medline
60. Repetto E, Yoon IS, Zheng H, Kang DE (2007) Presenilin 1 regulates epider-mal growth factor receptor turnover and signaling in the endosomallysosomal pathway. J Biol Chem 282:31504-31516. CrossRef Medline
61. Roberts GW, Gentleman SM, Lynch A, Graham DI (1991) beta A4 amyloid protein deposition in brain after head trauma. Lancet 338:1422-1423. CrossRef Medline
62. Rodrigues EM, Weissmiller AM, Goldstein LS (2012) Enhancedβ-secretase processing alters APP axonal transport and leads to axonal defects. Hum Mol Genet 21:4587-4601. CrossRef Medline
63. Rosette C, KarinM (1996) Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors. Science 274:1194-1197. CrossRef Medline
64. Rusu P, Jansen A, Soba P, Kirsch J, Löwer A, Merdes G, Kuan YH, Jung A, Beyreuther K, Kjaerulff O, Kins S (2007) Axonal accumulation of synaptic markers in APP transgenic Drosophila depends on the NPTY motif and is paralleled by defects in synaptic plasticity. Eur J Neurosci 25:1079-1086. CrossRef Medline
65. Satpute-Krishnan P, DeGiorgis JA, Conley MP, Jang M, Bearer EL (2006) A peptide zipcode sufficient for anterograde transport within amyloid precursor protein. Proc Natl Acad Sci U S A 103:16532-16537. CrossRef Medline
66. Scott JN, Parhad IM, Clark AW (1991) Beta-amyloid precursor protein gene is differentially expressed in axotomized sensory and motor systems. Brain Res Mol Brain Res 10:315-325. CrossRef Medline
67. Sheng JG, Price DL, Koliatsos VE (2003) The beta-amyloid-related proteins presenilin 1 and BACE1 are axonally transported to nerve terminals in the brain. Exp Neurol 184:1053-1057. CrossRef Medline
68. Shi J, Yang SH, Stubley L, Day AL, Simpkins JW (2000) Hypoperfusion induces overexpression of beta-amyloid precursor protein mRNA in a focal ischemic rodent model. Brain Res 853:1-4. CrossRef Medline
69. Skovronsky DM, Pijak DS, Doms RW, Lee VM (2000) A distinct ER/IC gamma-secretase competes with the proteasome for cleavage of APP. Biochemistry 39:810-817. CrossRef Medline
70. Smith DH, Chen XH, Iwata A, Graham DI (2003) Amyloid beta accumulation in axons after traumatic brain injury in humans. J Neurosurg 98: 1072-1077. CrossRef Medline
71. Somosy Z (2000) Radiation response of cell organelles. Micron 31:165-181. CrossRef Medline
72. Steuble M, Gerrits B, Ludwig A, Mateos JM, Diep TM, Tagaya M, Stephan A, Schätzle P, Kunz B, Streit P, Sonderegger P (2010) Molecular characterization of a trafficking organelle: dissecting the axonal paths of calsyntenin-1 transport vesicles. Proteomics 10:3775-3788. CrossRef Medline
73. Steuble M, Diep TM, Schätzle P, Ludwig A, Tagaya M, Kunz B, Sonderegger P (2012) Calsyntenin-1 shelters APP from proteolytic processing during anterograde axonal transport. Biol Open 1:761-774. CrossRef Medline
74. Stokin GB, Goldstein LS (2006) Axonal transport and Alzheimer's disease. Annu Rev Biochem 75:607-627. CrossRef Medline
75. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, Mount SL, Raman R, Davies P, Masliah E, Williams DS, Goldstein LS (2005) Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307:1282-1288. CrossRef Medline
76. Szodorai A, Kuan YH, Hunzelmann S, Engel U, Sakane A, Sasaki T, Takai Y, Kirsch J, Müller U, Beyreuther K, Brady S, Morfini G, Kins S (2009) APP anterograde transport requires Rab3A GTPase activity for assembly of the transport vesicle. J Neurosci 29:14534-14544. CrossRef Medline
77. Szpankowski L, Encalada SE, Goldstein LS (2012) Subpixel colocalization reveals amyloid precursor protein-dependent kinesin-1 and dynein association with axonal vesicles. Proc Natl Acad Sci U S A 109:8582-8587. CrossRef Medline
78. Takamori S, Holt M, Stenius K, Lemke EA, Grønborg M, Riedel D, Urlaub H, Schenck S, Brügger B, Ringler P, Müller SA, Rammner B, Gräter F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmüller H, Heuser J, et al. (2006) Molecular anatomy of a trafficking organelle. Cell 127:831-846. CrossRef Medline
79. Thinakaran G, Koo EH (2008) Amyloid precursor protein trafficking, processing, and function. J Biol Chem 283:29615-29619. CrossRef Medline
80. Tienari PJ, De Strooper B, Ikonen E, Simons M, Weidemann A, Czech C, Hartmann T, Ida N, Multhaup G, Masters CL, Van Leuven F, Beyreuther K, Dotti CG (1996) The beta-amyloid domain is essential for axonal sorting of amyloid precursor protein. EMBO J 15:5218-5229. Medline
81. Tokuda T, Kametani F, Tanaka K, Sahara N, Ikeda S, Yanagisawa N (1996) Amyloid beta protein and its 3-kDa fragment are present in the axoplasm fraction of the white matter in human brain. Biochem Biophys Res Commun 223:165-169. CrossRef Medline
82. Vagnoni A, Perkinton MS, Gray EH, Francis PT, Noble W, Miller CC (2012) Calsyntenin-1 mediates axonal transport of the amyloid precursor protein and regulates Aβ production. Hum Mol Genet 21:2845-2854. CrossRef Medline
83. Van den Heuvel C, Blumbergs PC, Finnie JW, Manavis J, Jones NR, Reilly PL, Pereira RA (1999) Upregulation of amyloid precursor protein messenger RNA in response to traumatic brain injury: an ovine head impact model. Exp Neurol 159:441-450. CrossRef Medline
84. Vogt L, Schrimpf SP, Meskenaite V, Frischknecht R, Kinter J, Leone DP, Ziegler U, Sonderegger P (2001) Calsyntenin-1, a proteolytically processed postsynaptic membrane protein with a cytoplasmic calciumbinding domain. Mol Cell Neurosci 17:151-166. CrossRef Medline
85. Volknandt W, Karas M (2012) Proteomic analysis of the presynaptic active zone. Exp Brain Res 217:449-461. CrossRef Medline
86. Weidemann A, König 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. CrossRef Medline
87. Yamazaki T, Koo EH, Selkoe DJ (1996) Trafficking of cell-surface amyloid beta-protein precursor. II. Endocytosis, recycling and lysosomal targeting detected by immunolocalization. J Cell Sci 109:999-1008. Medline
88. Zhang H, Ma Q, Zhang YW, Xu H (2012) Proteolytic processing of Alzheimer's β-amyloid precursor protein. J Neurochem 120 [Suppl 1]:9-21. CrossRef Medline