Genetic Analysis of a Novel Tubulin Mutation That Redirects Synaptic Vesicle Targeting and Causes Neurite Degeneration in C. elegans

PLoS Genetics

Volumn 10, Issue 11, 2014, Pages

  Hsu, Jiun Min ^a   Chen, Chun Hao ^a   Chen, Yen Chih ^a   McDonald, Kent L ^b   Gurling, Mark ^b,d   Lee, Albert ^c   Garriga, Gian ^b   Pan, Chun Liang ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; DYNEIN ADENOSINE TRIPHOSPHATASE; GLUTAMIC ACID; GLYCINE; MOLECULAR MOTOR; TUBULIN; CAENORHABDITIS ELEGANS PROTEIN; MEC-12 PROTEIN, C ELEGANS;

ARTICLE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DENDRITE; ELECTRON MICROSCOPY; GAIN OF FUNCTION MUTATION; GENE MUTATION; GENETIC ANALYSIS; MECHANICAL STRESS; MICROTUBULE; MISSENSE MUTATION; MUSCLE CONTRACTION; MUTAGENESIS; NERVE DEGENERATION; NERVE FIBER; NERVE FIBER DEGENERATION; NEURITE; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN TARGETING; SEDIMENTATION; SINGLE NUCLEOTIDE POLYMORPHISM; SYNAPSE VESICLE; WILD TYPE; ANIMAL; EXOCYTOSIS; GENETICS; HUMAN; METABOLISM; PATHOLOGY; SYNAPTIC TRANSMISSION;

CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DENDRITES; DYNEINS; EXOCYTOSIS; HUMANS; MICROTUBULES; MUTATION, MISSENSE; NERVE DEGENERATION; NEURITES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; TUBULIN;

EID: 84912124647     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004715     Document Type: Article

References (52)

1. Hirokawa N, Niwa S, Tanaka Y, (2010) Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 68: 610–638.
2. Conde C, Caceres A, (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10: 319–332.
3. Kapitein LC, Schlager MA, Kuijpers M, Wulf PS, van Spronsen M, et al. (2010) Mixed microtubules steer dynein-driven cargo transport into dendrites. Curr Biol 20: 290–299.
4. Rolls MM, (2011) Neuronal polarity in Drosophila: sorting out axons and dendrites. Dev Neurobiol 71: 419–429.
5. Maniar TA, Kaplan M, Wang GJ, Shen K, Wei L, et al. (2011) UNC-33 (CRMP) and ankyrin organize microtubules and localize kinesin to polarize axon-dendrite sorting. Nat Neurosci 15: 48–56.
6. Yan J, Chao DL, Toba S, Koyasako K, Yasunaga T, et al. (2013) Kinesin-1 regulates dendrite microtubule polarity in Caenorhabditis elegans. Elife 2: e00133.
7. Ou CY, Poon VY, Maeder CI, Watanabe S, Lehrman EK, et al. (2010) Two cyclin-dependent kinase pathways are essential for polarized trafficking of presynaptic components. Cell 141: 846–858.
8. Goodwin PR, Sasaki JM, Juo P, (2012) Cyclin-dependent kinase 5 regulates the polarized trafficking of neuropeptide-containing dense-core vesicles in Caenorhabditis elegans motor neurons. J Neurosci 32: 8158–8172.
9. Koushika SP, Schaefer AM, Vincent R, Willis JH, Bowerman B, et al. (2004) Mutations in Caenorhabditis elegans cytoplasmic dynein components reveal specificity of neuronal retrograde cargo. J Neurosci 24: 3907–3916.
10. Mizuno N, Toba S, Edamatsu M, Watai-Nishii J, Hirokawa N, et al. (2004) Dynein and kinesin share an overlapping microtubule-binding site. EMBO J 23: 2459–2467.
11. Kikkawa M, Hirokawa N, (2006) High-resolution cryo-EM maps show the nucleotide binding pocket of KIF1A in open and closed conformations. EMBO J 25: 4187–4194.
12. Redwine WB, Hernandez-Lopez R, Zou S, Huang J, Reck-Peterson SL, et al. (2012) Structural basis for microtubule binding and release by dynein. Science 337: 1532–1536.
13. Uchimura S, Oguchi Y, Hachikubo Y, Ishiwata S, Muto E, (2010) Key residues on microtubule responsible for activation of kinesin ATPase. EMBO J 29: 1167–1175.
14. Tischfield MA, Baris HN, Wu C, Rudolph G, Van Maldergem L, et al. (2010) Human TUBB3 mutations perturb microtubule dynamics, kinesin interactions, and axon guidance. Cell 140: 74–87.
15. Niwa S, Takahashi H, Hirokawa N, (2013) beta-Tubulin mutations that cause severe neuropathies disrupt axonal transport. EMBO J 32: 1352–1364.
16. Chalfie M.; Sulston J, (1981) Development Genetics of the Mechanosensory Neurons of C. elegans. Dev Biol 82: 358–370.
17. Fukushige T, Siddiqui ZK, Chou M, Culotti JG, Gogonea CB, et al. (1999) MEC-12, an alpha-tubulin required for touch sensitivity in C. elegans. J Cell Sci 112: 395–403.
18. Goodman MB, (2006) Mechanosensation. WormBook 6: 1–14.
19. Bounoutas A, Zheng Q, Nonet ML, Chalfie M (2009) mec-15 encodes an F-box protein required for touch receptor neuron mechanosensation, synapse formation and development. Genetics 183: : 607–617, 601SI-604SI.
20. Zheng Q, Schaefer AM, Nonet ML, (2011) Regulation of C. elegans presynaptic differentiation and neurite branching via a novel signaling pathway initiated by SAM-10. Development 138: 87–96.
21. Topalidou I, Keller C, Kalebic N, Nguyen KC, Somhegyi H, et al. (2012) Genetically separable functions of the MEC-17 tubulin acetyltransferase affect microtubule organization. Curr Biol 22: 1057–1065.
22. Krieg M, Dunn AR, Goodman MB, (2014) Mechanical control of the sense of touch by beta-spectrin. Nat Cell Biol 16: 224–233.
23. Pan CL, Peng CY, Chen CH, McIntire S, (2011) Genetic analysis of age-dependent defects of the Caenorhabditis elegans touch receptor neurons. Proc Natl Acad Sci U S A 108: 9274–9279.
24. Siddiqui SS, Aamodt E, Rastinejad F, Culotti J, (1989) Anti-tubulin monoclonal antibodies that bind to specific neurons in Caenorhabditis elegans. J Neurosci 9: 2963–2972.
25. Savage C, Xue Y, Mitani S, Hall D, Zakhary R, et al. (1994) Mutations in the Caenorhabditis elegans beta-tubulin gene mec-7: effects on microtubule assembly and stability and on tubulin autoregulation. J Cell Sci 107: 2165–2175.
26. Ghosh-Roy A, Goncharov A, Jin Y, Chisholm AD, (2012) Kinesin-13 and tubulin posttranslational modifications regulate microtubule growth in axon regeneration. Dev Cell 23: 716–728.
27. Neumann BH, M A, (2014) Loss of MEC-17 Leads to Microtubule Instability and Axonal Degeneration. Cell Reports 6: 93–103.
28. Kimura Y, Kurabe N, Ikegami K, Tsutsumi K, Konishi Y, et al. (2010) Identification of tubulin deglutamylase among Caenorhabditis elegans and mammalian cytosolic carboxypeptidases (CCPs). J Biol Chem 285: 22936–22941.
29. O'Hagan R, Piasecki BP, Silva M, Phirke P, Nguyen KC, et al. (2011) The tubulin deglutamylase CCPP-1 regulates the function and stability of sensory cilia in C. elegans. Curr Biol 21: 1685–1694.
30. Gonczy P, Pichler S, Kirkham M, Hyman AA, (1999) Cytoplasmic dynein is required for distinct aspects of MTOC positioning, including centrosome separation, in the one cell stage Caenorhabditis elegans embryo. J Cell Biol 147: 135–150.
31. Konishi Y, Setou M, (2009) Tubulin tyrosination navigates the kinesin-1 motor domain to axons. Nat Neurosci 12: 559–567.
32. Ikegami K, Heier RL, Taruishi M, Takagi H, Mukai M, et al. (2007) Loss of alpha-tubulin polyglutamylation in ROSA22 mice is associated with abnormal targeting of KIF1A and modulated synaptic function. Proc Natl Acad Sci U S A 104: 3213–3218.
33. Goshima Y, Nakamura F, Strittmatter P, Strittmatter SM, (1995) Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 376: 509–514.
34. Otsuka AJ, Franco R, Yang B, Shim KH, Tang LZ, et al. (1995) An ankyrin-related gene (unc-44) is necessary for proper axonal guidance in Caenorhabditis elegans. J Cell Biol 129: 1081–1092.
35. Tischfield MA, Cederquist GY, Gupta ML, JrEngle EC, (2011) Phenotypic spectrum of the tubulin-related disorders and functional implications of disease-causing mutations. Curr Opin Genet Dev 21: 286–294.
36. Simons C, Wolf NI, McNeil N, Caldovic L, Devaney JM, et al. (2013) A de novo mutation in the beta-tubulin gene TUBB4A results in the leukoencephalopathy hypomyelination with atrophy of the basal ganglia and cerebellum. Am J Hum Genet 92: 767–773.
37. Lohmann K, Wilcox RA, Winkler S, Ramirez A, Rakovic A, et al. (2013) Whispering dysphonia (DYT4 dystonia) is caused by a mutation in the TUBB4 gene. Ann Neurol 73: 537–545.
38. Keays DA, Tian G, Poirier K, Huang GJ, Siebold C, et al. (2007) Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell 128: 45–57.
39. Hammarlund M, Jorgensen EM, Bastiani MJ, (2007) Axons break in animals lacking beta-spectrin. J Cell Biol 176: 269–275.
40. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94.
41. Mello CC, Kramer JM, Stinchcomb D, Ambros V, (1991) Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10: 3959–3970.
42. Hilliard MA, Bargmann CI, (2006) Wnt signals and frizzled activity orient anterior-posterior axon outgrowth in C. elegans. Dev Cell 10: 379–390.
43. Prasad BC, Clark SG, (2006) Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans. Development 133: 1757–1766.
44. Pan CL, Baum PD, Gu M, Jorgensen EM, Clark SG, et al. (2008) C. elegans AP-2 and retromer control Wnt signaling by regulating mig-14/Wntless. Dev Cell 14: 132–139.
45. Davis MW, Hammarlund M, Harrach T, Hullett P, Olsen S, et al. (2005) Rapid single nucleotide polymorphism mapping in C. elegans. BMC Genomics 6: 118.
46. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J, (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2 RESEARCH0002.
47. Calixto A, Chelur D, Topalidou I, Chen X, Chalfie M, (2010) Enhanced neuronal RNAi in C. elegans using SID-1. Nat Methods 7: 554–559.
48. McDonald KL, Webb RI, (2011) Freeze substitution in 3 hours or less. J Microsc 243: 227–233.
49. Reynolds ES, (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17: 208–212.
50. Finney M, Ruvkun G, (1990) The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63: 895–905.
51. Lye RJ, Porter ME, Scholey JM, McIntosh JR, (1987) Identification of a microtubule-based cytoplasmic motor in the nematode C. elegans. Cell 51: 309–318.
52. Kumar J, Choudhary BC, Metpally R, Zheng Q, Nonet ML, et al. (2010) The Caenorhabditis elegans Kinesin-3 motor UNC-104/KIF1A is degraded upon loss of specific binding to cargo. PLoS Genet 6: e1001200.