Non-centrosomal nucleation mediated by augmin organizes microtubules in post-mitotic neurons and controls axonal microtubule polarity

Nature Communications

Volumn 7, Issue , 2016, Pages

  Sánchez Huertas, Carlos ^a,f   Freixo, Francisco ^a   Viais, Ricardo ^a   Lacasa, Cristina ^a   Soriano, Eduardo ^b,c,d,e   Lüders, Jens ^a  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^f Centre National de la Recherche Scientifique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ORGANELLE; CHROMOSOME; CYTOPLASM; GROWTH RATE; NEUROLOGY; NUCLEATION; PHYSIOLOGICAL RESPONSE;

AXON; GENE DISRUPTION; GENE INACTIVATION; HUMAN; MICROTUBULE; MITOSIS; NEURITE; ANIMAL; CELL POLARITY; CENTROSOME; CYTOLOGY; METABOLISM; MICROTUBULE ORGANIZING CENTER; MOUSE; NERVE CELL; NERVE FIBER TRANSPORT; NERVOUS SYSTEM DEVELOPMENT; SPINDLE POLE;

MICROTUBULE ASSOCIATED PROTEIN; MULTIPROTEIN COMPLEX; TUBG1 PROTEIN, MOUSE; TUBULIN;

ANIMALS; AXONAL TRANSPORT; AXONS; CELL POLARITY; CENTROSOME; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULE-ORGANIZING CENTER; MICROTUBULES; MULTIPROTEIN COMPLEXES; NEURITES; NEUROGENESIS; NEURONS; SPINDLE POLES; TUBULIN;

EID: 84978851256     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12187     Document Type: Article

References (69)

1. Conde, C. & Cáceres, A. Microtubule assembly, organization and dynamics in axons and dendrites. Nat. Rev. Neurosci. 10, 319-332 (2009).
2. Dent, E. W., Merriam, E. B. & Hu, X. The dynamic cytoskeleton: backbone of dendritic spine plasticity. Curr. Opin. Neurobiol. 21, 175-181 (2011).
3. Franker, M. A. M. & Hoogenraad, C. C. Microtubule-based transport - basic mechanisms, traffic rules and role in neurological pathogenesis. J. Cell Sci. 126, 2319-2329 (2013).
4. Kuijpers, M. & Hoogenraad, C. C. Centrosomes, microtubules and neuronal development. Mol. Cell Neurosci. 48, 349-358 (2011).
5. Poulain, F. E. & Sobel, A. The microtubule network and neuronal morphogenesis: dynamic and coordinated orchestration through multiple players. Mol. Cell. Neurosci. 43, 15-32 (2010).
6. Yu, W., Centonze, V. E., Ahmad, F. J. & Baas, P. W. Microtubule nucleation and release from the neuronal centrosome. J. Cell Biol. 122, 349-359 (1993).
7. Baas, P. W. & Yu, W. A composite model for establishing the microtubule arrays of the neuron. Mol. Neurobiol. 12, 145-161 (1996).
8. Sharp, D. J., Yu, W. & Baas, P. W. Transport of dendritic microtubules establishes their nonuniform polarity orientation. J. Cell Biol. 130, 93-103 (1995).
9. Joshi, H. C. & Baas, P. W. A new perspective on microtubules and axon growth. J. Cell Biol. 121, 1191-1196 (1993).
10. Ahmad, F. J., Echeverri, C. J., Vallee, R. B. & Baas, P. W. Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. J. Cell Biol. 140, 391-401 (1998).
11. Lin, S., Liu, M., Mozgova, O. I., Yu, W. & Baas, P. W. Mitotic motors coregulate microtubule patterns in axons and dendrites. J. Neurosci. 32, 14033-14049 (2012).
12. Zheng, Y. et al. Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat. Cell Biol. 10, 1172-1180 (2008).
13. Stiess, M. et al. Axon extension occurs independently of centrosomal microtubule nucleation. Science 327, 704-707 (2010).
14. Basto, R. et al. Flies without centrioles. Cell 125, 1375-1386 (2006).
15. Nguyen, M. M., Stone, M. C. & Rolls, M. M. Microtubules are organized independently of the centrosome in Drosophila neurons. Neural Dev. 6, 38 (2011).
16. Yu, W. et al. The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. Mol. Biol. Cell 19, 1485-1498 (2008).
17. Sharp, D. J. & Ross, J. L. Microtubule-severing enzymes at the cutting edge. J. Cell Sci. 125, 2561-2569 (2012).
18. Teixidó-Travesa, N., Roig, J. & Lüders, J. The where, when and how of microtubule nucleation - one ring to rule them all. J. Cell Sci. 125, 4445-4456 (2012).
19. Leask, A., Obrietan, K. & Stearns, T. Synaptically coupled central nervous system neurons lack centrosomal gamma-tubulin. Neurosci. Lett. 229, 17-20 (1997).
20. Ori-McKenney, K. M., Jan, L. Y. & Jan, Y.-N. Golgi outposts shape dendrite morphology by functioning as sites of acentrosomal microtubule nucleation in neurons. Neuron 76, 921-930 (2012).
21. Yau, K. W. et al. Microtubule minus-end binding protein CAMSAP2 controls axon specification and dendrite development. Neuron 82, 1058-1073 (2014).
22. Nguyen, M. M. et al. G-tubulin controls neuronal microtubule polarity independently of Golgi outposts. Mol. Biol. Cell 25, 2039-2050 (2014).
23. Quassollo, G. et al. A RhoA signaling pathway regulates dendritic Golgi outpost formation. Curr. Biol. 25, 971-982 (2015).
24. Sánchez-Huertas, C. & Lüders, J. The augmin connection in the geometry of microtubule networks. Curr. Biol. 25, R294-R299 (2015).
25. Goshima, G., Mayer, M., Zhang, N., Stuurman, N. & Vale, R. D. Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J. Cell Biol. 181, 421-429 (2008).
26. Lawo, S. et al. HAUS, the 8-subunit human Augmin complex, regulates centrosome and spindle integrity. Curr. Biol. 19, 816-826 (2009).
27. Petry, S., Pugieux, C., Nédélec, F. J. & Vale, R. D. Augmin promotes meiotic spindle formation and bipolarity in Xenopus egg extracts. Proc. Natl Acad. Sci. USA 108, 14473-14478 (2011).
28. Petry, S., Groen, A. C., Ishihara, K., Mitchison, T. J. & Vale, R. D. Branching microtubule nucleation in Xenopus egg extracts mediated by Augmin and TPX2. Cell 152, 768-777 (2013).
29. Kamasaki, T. et al. Augmin-dependent microtubule nucleation at microtubule walls in the spindle. J. Cell Biol. 202, 25-33 (2013).
30. Khodjakov, A. & Rieder, C. L. The sudden recruitment of gamma-tubulin to the centrosome at the onset of mitosis and its dynamic exchange throughout the cell cycle, do not require microtubules. J. Cell Biol. 146, 585-596 (1999).
31. Fuller, S. D. et al. The core of the mammalian centriole contains gammatubulin. Curr. Biol. 5, 1384-1393 (1995).
32. Lüders, J., Patel, U. K. & Stearns, T. GCP-WD is a gamma-tubulin targeting factor required for centrosomal and chromatin-mediated microtubule nucleation. Nat. Cell Biol. 8, 137-147 (2006).
33. Haren, L. et al. NEDD1-dependent recruitment of the gamma-tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly. J. Cell Biol. 172, 505-515 (2006).
34. Witte, H., Neukirchen, D. & Bradke, F. Microtubule stabilization specifies initial neuronal polarization. J. Cell Biol. 180, 619-632 (2008).
35. Janke, C. & Kneussel, M. Tubulin post-translational modifications: encoding functions on the neuronal microtubule cytoskeleton. Trends Neurosci. 33, 362-372 (2010).
36. Baas, P.W. & Black, M. M. Individual microtubules in the axon consist of domains that differ in both composition and stability. J Cell Biol. 111, 495-509 (1990).
37. Sheng, Z.-H. & Cai, Q. Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat. Rev. Neurosci. 13, 77-93 (2012).
38. Uehara, R. et al. The augmin complex plays a critical role in spindle microtubule generation for mitotic progression and cytokinesis in human cells. Proc. Natl Acad. Sci. USA 106, 6998-7003 (2009).
39. Zhu, H., Coppinger, J. A., Jang, C.-Y., Yates, J. R. & Fang, G. FAM29A promotes microtubule amplification via recruitment of the NEDD1-gammatubulin complex to the mitotic spindle. J. Cell Biol. 183, 835-848 (2008).
40. Wang, Z. et al. Conserved motif of CDK5RAP2 mediates its localization to centrosomes and the Golgi complex. J. Biol. Chem. 285, 22658-22665 (2010).
41. Choi, Y.-K., Liu, P., Sze, S. K., Dai, C. & Qi, R. Z. CDK5RAP2 stimulates microtubule nucleation by the gamma-tubulin ring complex. J. Cell Biol. 191, 1089-1095 (2010).
42. Poirier, K. et al. Mutations in TUBG1, DYNC1H1, KIF5C and KIF2A cause malformations of cortical development and microcephaly. Nat. Genet. 45, 639-647 (2013).
43. Tischfield, M. A., Cederquist, G. Y., Gupta, M. L. & Engle, E. C. Phenotypic spectrum of the tubulin-related disorders and functional implications of disease-causing mutations. Curr. Opin. Genet. Dev. 21, 286-294 (2011).
44. Bahi-Buisson, N. et al. The wide spectrum of tubulinopathies: what are the key features for the diagnosis? Brain 137, 1676-1700 (2014).
45. Murata, T. et al. Microtubule-dependent microtubule nucleation based on recruitment of g-tubulin in higher plants. Nat. Cell Biol. 7, 961-968 (2005).
46. Liu, T. et al. Augmin triggers microtubule-dependent microtubule nucleation in interphase plant cells. Curr. Biol. 24, 2708-2713 (2014).
47. Meireles, A. M., Fisher, K. H., Colombié, N., Wakefield, J. G. & Ohkura, H. Wac: a new Augmin subunit required for chromosome alignment but not for acentrosomal microtubule assembly in female meiosis. J. Cell Biol. 184, 777-784 (2009).
48. Scheidecker, S. et al. Mutations in TUBGCP4 alter microtubule organization via the g-tubulin ring complex in autosomal-recessive microcephaly with chorioretinopathy. Am. J. Hum. Genet. 96, 666-674 (2015).
49. Martin, C.-A. et al. Mutations in PLK4, encoding a master regulator of centriole biogenesis, cause microcephaly, growth failure and retinopathy. Nat. Genet. 46, 1283-1292 (2014).
50. Puffenberger, E. G. et al. Genetic mapping and exome sequencing identify variants associated with five novel diseases. PLoS ONE 7, e28936 (2012).
51. Funahashi, Y., Namba, T., Nakamuta, S. & Kaibuchi, K. Neuronal polarization in vivo: growing in a complex environment. Curr. Opin. Neurobiol. 27, 215-223 (2014).
52. Walia, A. et al. GCP-WD mediates g-TuRC recruitment and the geometry of microtubule nucleation in interphase arrays of Arabidopsis. Curr. Biol. 24, 2548-2555 (2014).
53. Johmura, Y. et al. Regulation of microtubule-based microtubule nucleation by mammalian polo-like kinase 1. Proc. Natl Acad. Sci. USA 108, 11446-11451 (2011).
54. Lecland, N. & Lüders, J. The dynamics of microtubule minus ends in the human mitotic spindle. Nat. Cell Biol. 16, 770-778 (2014).
55. Marcette, J. D., Chen, J. J., Nonet, M. L. & Hobert, O. The Caenorhabditis elegans microtubule minus-end binding homolog PTRN-1 stabilizes synapses and neurites. Elife 3, e01637 (2014).
56. Yang, Y. et al. The microtubule minus-end-binding protein patronin/PTRN-1 is required for axon regeneration in C. elegans. Cell Rep. 9, 874-883 (2014).
57. Richardson, C. E. et al. PTRN-1, a microtubule minus end-binding CAMSAP homolog, promotes microtubule function in Caenorhabditis elegans neurons. Elife 3, e01498 (2014).
58. Nakamura, M., Ehrhardt, D. W. & Hashimoto, T. Microtubule and katanindependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nat. Cell Biol. 12, 1064-1070 (2010).
59. Shaw, S. L., Kamyar, R. & Ehrhardt, D. W. Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300, 1715-1718 (2003).
60. Baas, P. W. & Mozgova, O. I. A novel role for retrograde transport of microtubules in the axon. Cytoskeleton (Hoboken) 69, 416-425 (2012).
61. Hsia, K.-C. et al. Reconstitution of the augmin complex provides insights into its architecture and function. Nat. Cell Biol. 16, 852-863 (2014).
62. Yalgin, C. et al. Centrosomin represses dendrite branching by orienting microtubule nucleation. Nat. Neurosci. 18, 1437-1445 (2015).
63. Sanchez-Huertas, C. & Rico, B. CREB-dependent regulation of GAD65 transcription by BDNF/TrkB in cortical interneurons. Cereb. Cortex 21, 777-788 (2011).
64. Rubinson, D. A. et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet. 33, 401-406 (2003).
65. Izumi, N., Fumoto, K., Izumi, S. & Kikuchi, A. GSK-3beta regulates proper mitotic spindle formation in cooperation with a component of the gamma-tubulin ring complex, GCP5. J. Biol. Chem. 283, 12981-12991 (2008).
66. Teixidó-Travesa, N. et al. The gammaTuRC revisited: a comparative analysis of interphase and mitotic human gammaTuRC redefines the set of core components and identifies the novel subunit GCP8. Mol. Biol. Cell. 21, 3963-3972 (2010).
67. Box, G. E. P. & Cox, D. R. An analysis of transformations. J. R. Stat. Soc. Ser. B (Methodol.) 26, 211-252 (1964).
68. Gelman, A. & Hill, J. Data Analysis Using Regression and Multilevel/Hierarchical Models (Cambridge University Press, 2006).
69. Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biom. J. 50, 346-363 (2008).