Transport of a kinesin-cargo pair along microtubules into dendritic spines undergoing synaptic plasticity

Nature Communications

Volumn 7, Issue , 2016, Pages

  McVicker, Derrick P ^a   Awe, Adam M ^a   Richters, Karl E ^a   Wilson, Rebecca L ^a   Cowdrey, Diana A ^a   Hu, Xindao ^a   Chapman, Edwin R ^a   Dent, Erik W ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN; PROTEIN KIF1A; SYNAPTOTAGMIN; SYNAPTOTAGMIN IV; UNCLASSIFIED DRUG;

CELL ORGANELLE; CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; POLYMERIZATION; PROTEIN; SENSORY SYSTEM;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DENDRITIC SPINE; DIFFUSION; ENZYME LOCALIZATION; EXOCYTOSIS; HIPPOCAMPUS; MEMBRANE FUSION; MICROTUBULE; MICROTUBULE ASSEMBLY; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN TRANSPORT; RAT;

EID: 84988650889     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12741     Document Type: Article

References (39)

1. Hammer, J. A. 3rd & Sellers, J. R. Walking to work: Roles for class V myosins as cargo transporters. Nat. Rev. Mol. Cell Biol. 13, 13-26 (2012).
2. Correia, S. S. et al. Motor protein-dependent transport of AMPA receptors into spines during long-term potentiation. Nat. Neurosci. 11, 457-466 (2008).
3. Wang, Z. et al. Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 135, 535-548 (2008).
4. Esteves da Silva, M. et al. Positioning of AMPA receptor-containing endosomes regulates synapse architecture. Cell Rep. 13, 933-943 (2015).
5. Wagner, W., Brenowitz, S. D. & Hammer, J. A. 3rd Myosin-Va transports the endoplasmic reticulum into the dendritic spines of Purkinje neurons. Nat. Cell Biol. 13, 40-48 (2011).
6. Gu, J., Firestein, B. L. & Zheng, J. Q. Microtubules in dendritic spine development. J. Neurosci. 28, 12120-12124 (2008).
7. Hu, X., Viesselmann, C., Nam, S., Merriam, E. & Dent, E. W. Activitydependent dynamic microtubule invasion of dendritic spines. J. Neurosci. 28, 13094-13105 (2008).
8. Jaworski, J. et al. Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61, 85-100 (2009).
9. Hu, X. et al. BDNF-induced increase of PSD-95 in dendritic spines requires dynamic microtubule invasions. J. Neurosci. 31, 15597-15603 (2011).
10. Cai, Q., Pan, P. Y. & Sheng, Z. H. Syntabulin-kinesin-1 family member 5B-mediated axonal transport contributes to activity-dependent presynaptic assembly. J. Neurosci. 27, 7284-7296 (2007).
11. Tanaka, Y. et al. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93, 1147-1158 (1998).
12. Guillaud, L., Setou, M. & Hirokawa, N. KIF17 dynamics and regulation of NR2B trafficking in hippocampal neurons. J. Neurosci. 23, 131-140 (2003).
13. Guillaud, L., Wong, R. & Hirokawa, N. Disruption of KIF17-Mint1 interaction by CaMKII-dependent phosphorylation: A molecular model of kinesin-cargo release. Nat. Cell Biol. 10, 19-29 (2008).
14. Lo, K. Y., Kuzmin, A., Unger, S. M., Petersen, J. D. & Silverman, M. A. KIF1A is the primary anterograde motor protein required for the axonal transport of dense-core vesicles in cultured hippocampal neurons. Neurosci. Lett. 491, 168-173 (2011).
15. Ryan, X. P. et al. The Rho-specific GEF Lfc interacts with neurabin and spinophilin to regulate dendritic spine morphology. Neuron 47, 85-100 (2005).
16. Hammond, J. W., Blasius, T. L., Soppina, V., Cai, D. & Verhey, K. J. Autoinhibition of the kinesin-2 motor KIF17 via dual intramolecular mechanisms. J. Cell Biol. 189, 1013-1025 (2010).
17. Hammond, J. W. et al. Mammalian Kinesin-3 motors are dimeric in vivo and move by processive motility upon release of autoinhibition. PLoS Biol. 7, e72 (2009).
18. Jenkins, B., Decker, H., Bentley, M., Luisi, J. & Banker, G. A novel split kinesin assay identifies motor proteins that interact with distinct vesicle populations. J. Cell Biol. 198, 749-761 (2012).
19. Kondo, M., Takei, Y. & Hirokawa, N. Motor protein KIF1A is essential for hippocampal synaptogeness and learning enhancement in an enriched environment. Neuron 73, 743-757 (2012).
20. Okada, Y., Yamazaki, H., Sekineaizawa, Y. & Hirokawa, N. The neuron-specific kinesin superfamily protein kif1a is a unique monomeric motor for anterograde axonal-transport of synaptic vesicle precursors. Cell 81, 769-780 (1995).
21. Arthur, C. P., Dean, C., Pagratis, M., Chapman, E. R. & Stowell, M. H. Loss of synaptotagmin IV results in a reduction in synaptic vesicles and a distortion of the Golgi structure in cultured hippocampal neurons. Neuroscience 167, 135-142 (2010).
22. Dean, C. et al. Synaptotagmin-IV modulates synaptic function and long-term potentiation by regulating BDNF release. Nat. Neurosci. 12, 767-776 (2009).
23. Liu, J. S. et al. Molecular basis for specific regulation of neuronal kinesin-3 motors by doublecortin family proteins. Mol. Cell 47, 707-721 (2012).
24. Yonekawa, Y. et al. Defect in synaptic vesicle precursor transport and neuronal cell death in KIF1A motor protein-deficient mice. J. Cell Biol. 141, 431-441 (1998).
25. Merriam, E. B. et al. Dynamic microtubules promote synaptic NMDA receptor-dependent spine enlargement. PLoS ONE 6, e27688 (2011).
26. Merriam, E. B. et al. Synaptic regulation of microtubule dynamics in dendritic spines by calcium, f-actin, and drebrin. J. Neurosci. 33, 16471-16482 (2013).
27. Lu, Y., Christian, K. & Lu, B. BDNF: A key regulator for protein synthesisdependent LTP and long-term memory? Neurobiol. Learn. Mem. 89, 312-323 (2008).
28. Wang, H. L., Zhang, Z., Hintze, M. & Chen, L. Decrease in calcium concentration triggers neuronal retinoic acid synthesis during homeostatic synaptic plasticity. J. Neurosci. 31, 17764-17771 (2011).
29. Sankaranarayanan, S., De Angelis, D., Rothman, J. E. & Ryan, T. A. The use of pHluorins for optical measurements of presynaptic activity. Biophys. J. 79, 2199-2208 (2000).
30. Dean, C. et al. Axonal and dendritic synaptotagmin isoforms revealed by a pHluorin-syt functional screen. Mol. Biol. Cell 23, 1715-1727 (2012).
31. Stepanova, T. et al. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23, 2655-2664 (2003).
32. Lee, J. R. et al. Characterization of the movement of the kinesin motor KIF1A in living cultured neurons. J. Biol. Chem. 278, 2624-2629 (2003).
33. McVicker, D. P., Millette, M. M. & Dent, E. W. Signaling to the microtubule cytoskeleton: An unconventional role for CaMKII. Dev. Neurobiol. 75, 423-434 (2015).
34. Dent, E. W. et al. Filopodia are required for cortical neurite initiation. Nat. Cell Biol. 9, 1347-1359 (2007).
35. Kaech, S. & Banker, G. Culturing hippocampal neurons. Nat. Protoc. 1, 2406-2415 (2006).
36. Chapleau, C. A., Carlo, M. E., Larimore, J. L. & Pozzo-Miller, L. The actions of BDNF on dendritic spine density and morphology in organotypic slice cultures depend on the presence of serum in culture media. J. Neurosci. Methods 169, 182-190 (2008).
37. Dunn, A. R., Kad, N. M., Nelson, S. R., Warshaw, D. M. & Wallace, S. S. Single Qdot-labeled glycosylase molecules use a wedge amino acid to probe for lesions while scanning along DNA. Nucleic Acids Res. 39, 7487-7498 (2011).
38. Kad, N. M., Wang, H., Kennedy, G. G., Warshaw, D. M. & Van Houten, B. Collaborative dynamic DNA scanning by nucleotide excision repair proteins investigated by single-molecule imaging of quantum-dot-labeled proteins. Mol. Cell 37, 702-713 (2010).
39. Saxton, M. J. & Jacobson, K. Single-particle tracking: Applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct. 26, 373-399 (1997).