The kinesin-3, Unc-104 regulates dendrite morphogenesis and synaptic development in Drosophila

Genetics

Volumn 195, Issue 1, 2013, Pages 59-72

  Kern, Jeannine V ^a   Zhang, Yao V ^a,b   Kramer, Stella ^a   Brenman, Jay E ^c   Rasse, Tobias M ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; KIF1A PROTEIN; KINESIN 3; MOLECULAR MOTOR; UNC 104 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTONOMIC NEUROPATHY; CONFOCAL MICROSCOPE; DENDRITE; DROSOPHILA; EMBRYO DEVELOPMENT; GENE MUTATION; HEREDITARY MOTOR SENSORY NEUROPATHY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LOCOMOTION; MORPHOGENESIS; NERVE CELL PLASTICITY; NEUROMUSCULAR SYNAPSE; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; REGULATORY MECHANISM; SYNAPTOGENESIS;

FHA DOMAIN; HEREDITARY SPASTIC PARAPLEGIA; KINESIN-3; SYNAPSE;

AMINO ACID SEQUENCE; ANIMALS; CELL GROWTH PROCESSES; DENDRITES; DROSOPHILA; DROSOPHILA PROTEINS; KINESIN; LOCOMOTION; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; MUTATION, MISSENSE; NEUROMUSCULAR JUNCTION;

EID: 84883767439     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.113.151639     Document Type: Article

References (52)

1. Barkus, R. V., O. Klyachko, D. Horiuchi, B. J. Dickson, and W. M. Saxton, 2008 Identification of an axonal kinesin-3 motor for fast anterograde vesicle transport that facilitates retrograde transport of neuropeptides. Mol. Biol. Cell 19: 274-283.
2. Bayat, V., M. Jaiswal, and H. J. Bellen, 2011 The BMP signaling pathway at the Drosophila neuromuscular junction and its links to neurodegenerative diseases. Curr. Opin. Neurobiol. 21: 182-188.
3. Bliss, T. V., and T. Lomo, 1973 Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232: 331-356.
4. Cai, Q., P. Y. Pan, and Z. H. Sheng, 2007 Syntabulin-kinesin-1 family member 5B-mediated axonal transport contributes to activity-dependent presynaptic assembly. J. Neurosci. 27: 7284-7296.
5. Clarke, G. L., J. Chen, and H. Nishimune, 2012 Presynaptic Active Zone Density during Development and Synaptic Plasticity. Front Mol Neurosci 5: 12.
6. Corty, M. M., B. J. Matthews, and W. B. Grueber, 2009 Molecules and mechanisms of dendrite development in Drosophila. Development 136: 1049-1061.
7. Dietzl, G., D. Chen, F. Schnorrer, K. C. Su, Y. Barinova et al., 2007 A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-156.
8. Eaton, B. A., and G. W. Davis, 2005 LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron 47: 695-708.
9. Eaton, B. A., R. D. Fetter, and G. W. Davis, 2002 Dynactin is necessary for synapse stabilization. Neuron 34: 729-741.
10. Erlich, Y., S. Edvardson, E. Hodges, S. Zenvirt, P. Thekkat et al., 2011 Exome sequencing and disease-network analysis of a single family implicate a mutation in KIF1A in hereditary spastic paraparesis. Genome Res. 21: 658-664.
11. Fuger, P., L. B. Behrends, S. Mertel, S. J. Sigrist, and T. M. Rasse, 2007 Live imaging of synapse development and measuring protein dynamics using two-color fluorescence recovery after photo-bleaching at Drosophila synapses. Nat. Protoc. 2: 3285-3298.
12. Fuger, P., V. Sreekumar, R. Schule, J. V. Kern, D. T. Stanchev et al., 2012 Spastic paraplegia mutation N256S in the neuronal microtubule motor KIF5A disrupts axonal transport in a Drosophila HSP model. PLoS Genet. 8: e1003066.
13. Gao, F. B., J. E. Brenman, L. Y. Jan, and Y. N. Jan, 1999 Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Dev. 13: 2549-2561.
14. Hall, D. H., and E. M. Hedgecock, 1991 Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65: 837-847.
15. Hall, D. H., and M. Treinin, 2011 How does morphology relate to function in sensory arbors? Trends Neurosci. 34: 443-451.
16. Hirokawa, N., and Y. Noda, 2008 Intracellular transport and kinesin superfamily proteins, KIFs: structure, function, and dynamics. Physiol. Rev. 88: 1089-1118.
17. Hirokawa, N., S. Niwa, and Y. Tanaka, 2010 Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 68: 610-638.
18. Hoogenraad, C. C., A. D. Milstein, I. M. Ethell, M. Henkemeyer, and M. Sheng, 2005 GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat. Neurosci. 8: 906-915.
19. Huo, L., Y. Yue, J. Ren, J. Yu, J. Liu et al., 2012 The CC1-FHA tandem as a central hub for controlling the dimerization and activation of kinesin-3 KIF1A. Structure 20: 1550-1561.
20. Hurd, D. D., and W. M. Saxton, 1996 Kinesin Mutations Cause Motor Neuron Disease Phenotypes by Disrupting Fast Axonal Transport in Drosophila. Genetics 144: 1075-1085.
21. + channel clustering, and vesicle release. Science 312: 1051-1054.
22. Klebe, S., A. Lossos, H. Azzedine, E. Mundwiller, R. Sheffer et al., 2012 KIF1A missense mutations in SPG30, an autosomal recessive spastic paraplegia: distinct phenotypes according to the nature of the mutations. Eur. J. Hum. Genet. 20: 645-649.
23. Kondo, M., Y. Takei, and N. Hirokawa, 2012 Motor protein KIF1A is essential for hippocampal synaptogenesis and learning enhancement in an enriched environment. Neuron 73: 743-757.
24. Mahr, A., and H. Aberle, 2006 The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr. Patterns 6: 299-309.
25. Marin-Padilla, M., 1972 Structural abnormalities of the cerebral cortex in human chromosomal aberrations: a Golgi study. Brain Res. 44: 625-629.
26. Marrus, S. B., S. L. Portman, M. J. Allen, K. G. Moffat, and A. DiAntonio, 2004 Differential localization of glutamate receptor subunits at the Drosophila neuromuscular junction. J. Neurosci. 24: 1406-1415.
27. Medina, P. M., L. L. Swick, R. Andersen, Z. Blalock, and J. E. Brenman, 2006 A novel forward genetic screen to identify mutations affecting larval neuronal dendrite development in Drosophila melanogaster. Genetics 172: 2325-2335.
28. Nangaku, M., R. Sato-Yoshitake, Y. Okada, Y. Noda, R. Takemura et al., 1994 KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 79: 1209-1220.
29. O'Farrell, F., S. S. Esfahani, Y. Engstrom, and P. Kylsten, 2008 Regulation of the Drosophila lin-41 homologue dappled by let-7 reveals conservation of a regulatory mechanism within the LIN-41 subclade. Dev. Dyn. 237: 196-208.
30. Ohashi, S., K. Koike, A. Omori, S. Ichinose, S. Ohara et al., 2002 Identification of mRNA/protein (mRNP) complexes containing Puralpha, mStaufen, fragile X protein, and myosin Va and their association with rough endoplasmic reticulum equipped with a kinesin motor. J. Biol. Chem. 277: 37804-37810.
31. Pack-Chung, E., P. T. Kurshan, D. K. Dickman, and T. L. Schwarz, 2007 A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport. Nat. Neurosci. 10: 980-989.
32. Parks, A. L., K. R. Cook, M. Belvin, N. A. Dompe, R. Fawcett et al., 2004 Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36: 288-292.
33. Puthanveettil, S. V., F. J. Monje, M. C. Miniaci, Y. B. Choi, K. A. Karl et al., 2008 A new component in synaptic plasticity: upregulation of kinesin in the neurons of the gill-withdrawal reflex. Cell 135: 960-973.
34. Qin, G., T. Schwarz, R. J. Kittel, A. Schmid, T. M. Rasse et al., 2005 Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of Drosophila. J. Neurosci. 25: 3209-3218.
35. Rasse, T. M., W. Fouquet, A. Schmid, R. J. Kittel, S. Mertel et al., 2005 Glutamate receptor dynamics organizing synapse formation in vivo. Nat. Neurosci. 8: 898-905.
36. Rieckhof, G. E., M. Yoshihara, Z. Guan, and J. T. Littleton, 2003 Presynaptic N-type calcium channels regulate synaptic growth. J. Biol. Chem. 278: 41099-41108.
37. Riviere, J. B., S. Ramalingam, V. Lavastre, M. Shekarabi, S. Holbert et al., 2011 KIF1A, an axonal transporter of synaptic vesicles, is mutated in hereditary sensory and autonomic neuropathy type 2. Am. J. Hum. Genet. 89: 219-230.
38. Ryder, E., M. Ashburner, R. Bautista-Llacer, J. Drummond, J. Webster et al., 2007 The DrosDel deletion collection: a Drosophila genomewide chromosomal deficiency resource. Genetics 177: 615-629.
39. Schmid, A., S. Hallermann, R. J. Kittel, O. Khorramshahi, A. M. Frolich et al., 2008 Activity-dependent site-specific changes of glutamate receptor composition in vivo. Nat. Neurosci. 11: 659-666.
40. Sherwood, N. T., Q. Sun, M. Xue, B. Zhang, and K. Zinn, 2004 Drosophila spastin regulates synaptic microtubule networks and is required for normal motor function. PLoS Biol. 2: e429.
41. Sweeney, S. T., and G. W. Davis, 2002 Unrestricted synaptic growth in spinster-a late endosomal protein implicated in TGF-beta-mediated synaptic growth regulation. Neuron 36: 403-416.
42. Thibault, S. T., M. A. Singer, W. Y. Miyazaki, B. Milash, N. A. Dompe et al., 2004 A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 36: 283-287.
43. Tsubouchi, A., J. C. Caldwell, and W. D. Tracey, 2012 Dendritic filopodia, Ripped Pocket, NOMPC, and NMDARs contribute to the sense of touch in Drosophila larvae. Curr. Biol. 22: 2124-2134.
44. van den Berg, R., and C. C. Hoogenraad, 2012 Molecular motors in cargo trafficking and synapse assembly. Adv. Exp. Med. Biol. 970: 173-196.
45. Verhey, K. J., and J. W. Hammond, 2009 Traffic control: regulation of kinesin motors. Nat. Rev. Mol. Cell Biol. 10: 765-777.
46. Verhey, K. J., N. Kaul, and V. Soppina, 2011 Kinesin assembly and movement in cells. Annu Rev Biophys 40: 267-288.
47. Vitureira, N., M. Letellier, and Y. Goda, 2011 Homeostatic synaptic plasticity: from single synapses to neural circuits. Curr. Opin. Neurobiol. 22: 516-521.
48. Wagh, D. A., T. M. Rasse, E. Asan, A. Hofbauer, I. Schwenkert et al., 2006 Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49: 833-844.
49. Wang, X., W. R. Shaw, H. T. Tsang, E. Reid, and C. J. O'Kane, 2007 Drosophila spichthyin inhibits BMP signaling and regulates synaptic growth and axonal microtubules. Nat. Neurosci. 10: 177-185.
50. Zhai, R. G., P. R. Hiesinger, T. W. Koh, P. Verstreken, K. L. Schulze et al., 2003 Mapping Drosophila mutations with molecularly defined P element insertions. Proc. Natl. Acad. Sci. USA 100: 10860-10865.
51. Zhang, Y., P. Fuger, S. B. Hannan, J. V. Kern, B. Lasky et al., 2010 In vivo imaging of intact Drosophila larvae at sub-cellular resolution. J. Vis. Exp. 10: pii: 2249.
52. Zhou, B., Q. Cai, Y. Xie, and Z. H. Sheng, 2012 Snapin Recruits Dynein to BDNF-TrkB Signaling Endosomes for Retrograde Axonal Transport and Is Essential for Dendrite Growth of Cortical Neurons. Cell Rep 2: 42-51.