Endogenous GSK-3/Shaggy regulates bidirectional axonal transport of the amyloid precursor protein

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Volumn 14, Issue 3, 2013, Pages 295-308

  Weaver, Carole ^a,c   Leidel, Christina ^b   Szpankowski, Lukasz ^a   Farley, Nicole M ^b   Shubeita, George T ^b   Goldstein, Lawrence S B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Alzheimer's; Amyloid precursor protein; Axonal transport; Dynein; GSK 3; Kinesin; Lipid droplets; Optical trap

Indexed keywords

AMYLOID PRECURSOR PROTEIN; FAT DROPLET; GLYCOGEN SYNTHASE KINASE 3; KINESIN 1;

ARTICLE; DROSOPHILA MELANOGASTER; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; LOSS OF FUNCTION MUTATION; MICROTUBULE; NERVE FIBER; NEUROMUSCULAR SYNAPSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TRANSPORT; WILD TYPE;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; AXONAL TRANSPORT; AXONS; DROSOPHILA; DROSOPHILA PROTEINS; DYNEINS; GLYCOGEN SYNTHASE KINASE 3; KINESIN; LIPID METABOLISM; PROTEIN TRANSPORT;

EID: 84873477336     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12037     Document Type: Article

References (73)

1. Stokin GB, Goldstein LS. Axonal transport and Alzheimer's disease. Annu Rev Biochem 2006;75:607-627.
2. Salinas S, Bilsland LG, Schiavo G. Molecular landmarks along the axonal route: axonal transport in health and disease. Curr Opin Cell Biol 2008;20:445-453.
3. Gunawardena S, Goldstein LS. Disruption of axonal transport and neuronal viability by amyloid precursor protein mutations in Drosophila. Neuron 2001;32:389-401.
4. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, Mount SL, Raman R, Davies P, Masliah E, Williams DS, Goldstein LS. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 2005;307:1282-1288.
5. Goldstein AY, Wang X, Schwarz TL. Axonal transport and the delivery of pre-synaptic components. Curr Opin Neurobiol 2008;18:495-503.
6. Ibanez CF. Message in a bottle: long-range retrograde signaling in the nervous system. Trends Cell Biol 2007;17:519-528.
7. Gross SP, Vershinin M, Shubeita GT. Cargo transport: two motors are sometimes better than one. Curr Biol 2007;17:R478-R486.
8. Ally S, Larson AG, Barlan K, Rice SE, Gelfand VI. Opposite-polarity motors activate one another to trigger cargo transport in live cells. J Cell Biol 2009;187:1071-1082.
9. Verhey KJ, Hammond JW. Traffic control: regulation of kinesin motors. Nat Rev Mol Cell Biol 2009;10:765-777.
10. Arimura N, Kimura T, Nakamuta S, Taya S, Funahashi Y, Hattori A, Shimada A, Menager C, Kawabata S, Fujii K, Iwamatsu A, Segal RA, Fukuda M, Kaibuchi K. Anterograde transport of TrkB in axons is mediated by direct interaction with Slp1 and Rab27. Dev Cell 2009;16:675-686.
11. Chen S, Owens GC, Crossin KL, Edelman DB. Serotonin stimulates mitochondrial transport in hippocampal neurons. Mol Cell Neurosci 2007;36:472-483.
12. Du J, Wei Y, Liu L, Wang Y, Khairova R, Blumenthal R, Tragon T, Hunsberger JG, Machado-Vieira R, Drevets W, Wang YT, Manji HK. A kinesin signaling complex mediates the ability of GSK- 3beta to affect mood-associated behaviors. Proc Natl Acad Sci USA 2010;107:11573-11578.
13. Morel M, Authelet M, Dedecker R, Brion JP. Glycogen synthase kinase-3beta and the p25 activator of cyclin dependent kinase 5 increase pausing of mitochondria in neurons. Neuroscience 2010;167:1044-1056.
14. Morfini G, Szebenyi G, Brown H, Pant HC, Pigino G, DeBoer S, Beffert U, Brady ST. A novel CDK5-dependent pathway for regulating GSK3 activity and kinesin-driven motility in neurons. EMBO J 2004;23:2235-2245.
15. Morfini G, Szebenyi G, Elluru R, Ratner N, Brady ST. Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J 2002;21:281-293.
16. Pigino G, Morfini G, Pelsman A, Mattson MP, Brady ST, Busciglio J. Alzheimer's presenilin 1 mutations impair kinesin-based axonal transport. J Neurosci 2003;23:4499-4508.
17. Hooper C, Killick R, Lovestone S. The GSK3 hypothesis of Alzheimer's disease. J Neurochem 2008;104:1433-1439.
18. Arimura N, Kaibuchi K. Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat Rev Neurosci 2007;8:194-205.
19. Peineau S, Bradley C, Taghibiglou C, Doherty A, Bortolotto ZA, Wang YT, Collingridge GL. The role of GSK-3 in synaptic plasticity. Br J Pharmacol 2008;153:S428-S437.
20. Gould TD, Picchini AM, Einat H, Manji HK. Targeting glycogen synthase kinase-3 in the CNS: implications for the development of new treatments for mood disorders. Curr Drug Targets 2006;7:1399-1409.
21. Jope RS, Roh MS. Glycogen synthase kinase-3 (GSK3) in psychiatric diseases and therapeutic interventions. Curr Drug Targets 2006;7:1421-1434.
22. Cuchillo-Ibanez I, Seereeram A, Byers HL, Leung KY, Ward MA, Anderton BH, Hanger DP. Phosphorylation of tau regulates its axonal transport by controlling its binding to kinesin. FASEB J 2008;22:3186-3195.
23. Arimura N, Hattori A, Kimura T, Nakamuta S, Funahashi Y, Hirotsune S, Furuta K, Urano T, Toyoshima YY, Kaibuchi K. CRMP-2 directly binds to cytoplasmic dynein and interferes with its activity. J Neurochem 2009;111:380-390.
24. Siegfried E, Chou TB, Perrimon N. Wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell 1992;71:1167-1179.
25. Hurd DD, Saxton WM. Kinesin mutations cause motor neuron disease phenotypes by disrupting fast axonal transport in Drosophila. Genetics 1996;144:1075-1085.
26. Bowman AB, Kamal A, Ritchings BW, Philp AV, McGrail M, Gindhart JG, Goldstein LS. Kinesin-dependent axonal transport is mediated by the Sunday driver (SYD) protein. Cell 2000;103:583-594.
27. Heslip TR, Theisen H, Walker H, Marsh JL. Shaggy and dishevelled exert opposite effects on Wingless and Decapentaplegic expression and on positional identity in imaginal discs. Development 1997;124:1069-1078.
28. Judd BH, Shen MW, Kaufman TC. The anatomy and function of a segment of the X chromosome of Drosophila melanogaster Genetics 1972;71:139-156.
29. Bourouis M, Heitzler P, el Messal M, Simpson P. Mutant Drosophila embryos in which all cells adopt a neural fate. Nature 1989;341:442-444.
30. Ruel L, Pantesco V, Lutz Y, Simpson P, Bourouis M. Functional significance of a family of protein kinases encoded at the shaggy locus in Drosophila. EMBO J 1993;12:1657-1669.
31. Yang W, Leystra-Lantz C, Strong MJ. Upregulation of GSK3beta expression in frontal and temporal cortex in ALS with cognitive impairment (ALSci). Brain Res 2008;1196:131-139.
32. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993;118:401-415.
33. Bourouis M. Targeted increase in shaggy activity levels blocks wingless signaling. Genesis 2002;34:99-102.
34. Harwood AJ. Regulation of GSK-3: a cellular multiprocessor. Cell 2001;105:821-824.
35. Martin M, Iyadurai SJ, Gassman A, Gindhart JG Jr, Hays TS, Saxton WM. Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. Mol Biol Cell 1999;10:3717-3728.
36. Kaether C, Skehel P, Dotti CG. Axonal membrane proteins are transported in distinct carriers: a two-color video microscopy study in cultured hippocampal neurons. Mol Biol Cell 2000;11:1213-1224.
37. Amaratunga A, Leeman SE, Kosik KS, Fine RE. Inhibition of kinesin synthesis in vivo inhibits the rapid transport of representative proteins for three transport vesicle classes into the axon. J Neurochem 1995;64:2374-2376.
38. Kamal A, Goldstein LS. Connecting vesicle transport to the cytoskeleton. Curr Opin Cell Biol 2000;12:503-508.
39. Kamal A, Almenar-Queralt A, LeBlanc JF, Roberts EA, Goldstein LS. Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 2001;414:643-648.
40. Reis GF, Yang G, Szpankowski L, Weaver C, Shah SB, Robinson JT, Hays TS, Danuser G, Goldstein LSB. Molecular motor function in axonal transport in vivo probed by genetic and computational analysis in Drosophila. Mol Biol Cell 2012;23:1700-1714.
41. Gunawardena S, Her LS, Brusch RG, Laymon RA, Niesman IR, Gordesky-Gold B, Sintasath L, Bonini NM, Goldstein LS. Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 2003;40:25-40.
42. Shyamala BV, Chopra A. Drosophila melanogaster chemosensory and muscle development: identification and properties of a novel allele of scalloped and of a new locus, SG18.1, in a Gal4 enhancer trap screen. J Genet 1999;78:87-97.
43. Fraley C, Raftery AE. Model-based clustering, discriminant analysis, and density estimation. J Amer Statist Assoc 2002;97:611-631.
44. Zhang YQ, Rodesch CK, Broadie K. Living synaptic vesicle marker: synaptotagmin-GFP. Genesis 2002;34:142-145.
45. Pack-Chung E, Kurshan PT, Dickman DK, Schwarz TL. A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport. Nat Neurosci 2007;10:980-989.
46. Barkus RV, Klyachko O, Horiuchi D, Dickson BJ, Saxton WM. Identification of an axonal kinesin-3 motor for fast anterograde vesicle transport that facilitates retrograde transport of neuropeptides. Mol Biol Cell 2008;19:274-283.
47. Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, Gaertig J, Verhey KJ. Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 2006;16:2166-2172.
48. Hall AC, Brennan A, Goold RG, Cleverley K, Lucas FR, Gordon- Weeks PR, Salinas PC. Valproate regulates GSK-3-mediated axonal remodeling and synapsin I clustering in developing neurons. Mol Cell Neurosci 2002;20:257-270.
49. Hall AC, Lucas FR, Salinas PC. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 2000;100:525-535.
50. Mimori-Kiyosue Y, Shiina N, Tsukita S. The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules. Curr Biol 2000;10:865-868.
51. Gross SP, Welte MA, Block SM, Wieschaus EF. Dynein-mediated cargo transport in vivo. A switch controls travel distance. J Cell Biol 2000;148:945-956.
52. Shubeita GT, Tran SL, Xu J, Vershinin M, Cermelli S, Cotton SL, Welte MA, Gross SP. Consequences of motor copy number on the intracellular transport of kinesin-1-driven lipid droplets. Cell 2008;135:1098-1107.
53. Xu J, Reddy BJ, Anand P, Shu Z, Cermelli S, Mattson MK, Tripathy SK, Hoss MT, James NS, King SJ, Huang L, Bardwell L, Gross SP. Casein kinase 2 reverses tail-independent inactivation of kinesin-1. Nat Commun 2012;3:754.
54. Larsen KS, Xu J, Cermelli S, Shu Z, Gross SP. BicaudalD actively regulates microtubule motor activity in lipid droplet transport. PLoS One 2008;3:e3763.
55. Pilling AD, Horiuchi D, Lively CM, Saxton WM. Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol Biol Cell 2006;17:2057-2068.
56. Brady ST, Pfister KK, Bloom GS. A monoclonal antibody against kinesin inhibits both anterograde and retrograde fast axonal transport in squid axoplasm. Proc Natl Acad Sci USA 1990;87:1061-1065.
57. Levi V, Serpinskaya AS, Gratton E, Gelfand V. Organelle transport along microtubules in Xenopus melanophores: evidence for cooperation between multiple motors. Biophys J 2006;90:318-327.
58. Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B, Mandelkow E. Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J Cell Biol 1998;143:777-794.
59. Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM. Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 2002;156:1051-1063.
60. Dixit R, Ross JL, Goldman YE, Holzbaur EL. Differential regulation of dynein and kinesin motor proteins by tau. Science 2008;319:1086-1089.
61. Seitz A, Kojima H, Oiwa K, Mandelkow EM, Song YH, Mandelkow E. Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J 2002;21:4896-4905.
62. Vershinin M, Carter BC, Razafsky DS, King SJ, Gross SP. Multiplemotor based transport and its regulation by Tau. Proc Natl Acad Sci USA 2007;104:87-92.
63. Vershinin M, Xu J, Razafsky DS, King SJ, Gross SP. Tuning microtubule-based transport through filamentous MAPs: the problem of dynein. Traffic 2008;9:882-892.
64. Stokin GB, Goldstein LS. Linking molecular motors to Alzheimer's disease. J Physiol Paris 2006;99:193-200.
65. Torroja L, Packard M, Gorczyca M, White K, Budnik V. The Drosophila beta-amyloid precursor protein homolog promotes synapse differentiation at the neuromuscular junction. J Neurosci 1999;19:7793-7803.
66. Huang HC, Klein PS. Multiple roles for glycogen synthase kinase- 3 as a drug target in Alzheimer's disease. Curr Drug Targets 2006;7:1389-1397.
67. Chuang DM, Manji HK. In search of the Holy Grail for the treatment of neurodegenerative disorders: has a simple cation been overlooked? Biol Psychiatry 2007;62:4-6.
68. Haghnia M, Cavalli V, Shah SB, Schimmelpfeng K, Brusch R, Yang G, Herrera C, Pilling A, Goldstein LS. Dynactin is required for coordinated bidirectional motility, but not for dynein membrane attachment. Mol Biol Cell 2007;18:2081-2089.
69. Cermelli S, Guo Y, Gross SP, Welte MA. The lipid-droplet proteome reveals that droplets are a protein-storage depot. Curr Biol 2006;16:1783-1795.
70. Welte MA, Gross SP, Postner M, Block SM, Wieschaus EF. Developmental regulation of vesicle transport in Drosophila embryos: forces and kinetics. Cell 1998;92:547-557.
71. Carter BC, Shubeita GT, Gross SP. Tracking single particles: a userfriendly quantitative evaluation. Phys Biol 2005;2:60-72.
72. Petrov DY, Mallik R, Shubeita GT, Vershinin M, Gross SP, Yu CC. Studying molecular motor-based cargo transport: what is real and what is noise? Biophys J 2007;92:2953-2963.
73. Leidel C, Longoria RA, Gutierrez FM, Shubeita GT. Measuring molecular motor forces in vivo: implications for tug-of-war models of bidirectional transport. Biophys J 2012;103:492-500.