Katanin p80, NuMA and cytoplasmic dynein cooperate to control microtubule dynamics

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Jin, Mingyue ^a   Pomp, Oz ^b   Shinoda, Tomoyasu ^c   Toba, Shiori ^a   Torisawa, Takayuki ^d,e   Furuta, Kenya ^d,e   Oiwa, Kazuhiro ^d,e,f   Yasunaga, Takuo ^e,g   Kitagawa, Daiju ^h   Matsumura, Shigeru ⁱ   Miyata, Takaki ^c   Tan, Thong Teck ^b   Reversade, Bruno ^b,j,k   Hirotsune, Shinji ^a  

^a OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d NATIONAL INSTITUTE OF INFORMATION AND COMMUNICATIONS TECHNOLOGY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^f UNIVERSITY OF HYOGO   (Japan)

^g KYUSHU INSTITUTE OF TECHNOLOGY   (Japan)

^h NATIONAL INSTITUTE OF GENETICS   (Japan)

ⁱ KYOTO UNIVERSITY   (Japan)

^j INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^k NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DYNEIN ADENOSINE TRIPHOSPHATASE; KATANIN P80, HUMAN; NUCLEAR PROTEIN; NUMA1 PROTEIN, MOUSE; SMALL INTERFERING RNA;

ANIMAL; FIBROBLAST; GENETICS; HELA CELL LINE; HUMAN; INBRED MOUSE STRAIN; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MICROTUBULE; MITOSIS; MOUSE; MUTATION; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM MALFORMATION; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATASES; ANIMALS; DYNEINS; FIBROBLASTS; HELA CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; MICE, INBRED STRAINS; MICROTUBULES; MITOSIS; MUTATION; NERVOUS SYSTEM MALFORMATIONS; NEUROGENESIS; NEURONS; NUCLEAR PROTEINS; RNA, SMALL INTERFERING;

EID: 85009442774     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep39902     Document Type: Article

References (46)

1. Gupta, A., Tsai, L. H., & Wynshaw-Boris, A. Life is A journey: A genetic look at neocortical development. Nature reviews. Genetics 3, 342-355 (2002
2. Barkovich, A. J., Guerrini, R., Kuzniecky, R. I., Jackson, G. D., & Dobyns, W. B. A developmental and genetic classification for malformations of cortical development: update 2012. Brain: A journal of neurology 135, 1348-1369 (2012
3. Thornton, G. K., & Woods, C. G. Primary microcephaly: do all roads lead to Rome?. Trends in genetics: TIG 25, 501-510 (2009
4. Mahmood, S., Ahmad, W., & Hassan, M. J. Autosomal Recessive Primary Microcephaly (MCPH): clinical manifestations, genetic heterogeneity and mutation continuum. Orphanet journal of rare diseases 6, 39 (2011
5. Wynshaw-Boris, A., Pramparo, T., Youn, Y. H., & Hirotsune, S. Lissencephaly: mechanistic insights from animal models and potential therapeutic strategies. Seminars in cell & developmental biology 21, 823-830 (2010
6. Reiner, O., et al. Isolation of A Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 364, 717-721 (1993
7. Hirotsune, S., et al. Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nature genetics 19, 333-339 (1998
8. Gleeson, J. G., et al. Doublecortin, A brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes A putative signaling protein. Cell 92, 63-72 (1998
9. Hong, S. E., et al. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nature genetics 26, 93-96 (2000
10. Poirier, K., et al. Large spectrum of lissencephaly and pachygyria phenotypes resulting from de novo missense mutations in tubulin alpha 1A (TUBA1A). Human mutation 28, 1055-1064 (2007
11. Bhat, V., et al. Mutations in WDR62, encoding A centrosomal and nuclear protein, in Indian primary microcephaly families with cortical malformations. Clinical genetics 80, 532-540 (2011
12. Bilguvar, K., et al. Whole-exome sequencing identifies recessive WDR62 mutations in severe brain malformations. Nature 467, 207-210 (2010
13. Alkuraya, F. S., et al. Human mutations in NDE1 cause extreme microcephaly with lissencephaly [corrected]. American journal of human genetics 88, 536-547 (2011
14. McNally, F. J., & Vale, R. D. Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 75, 419-429 (1993
15. McNally, K., Audhya, A., Oegema, K., & McNally, F. J. Katanin controls mitotic and meiotic spindle length. The Journal of cell biology 175, 881-891 (2006
16. Zhang, D., Rogers, G. C., Buster, D. W., & Sharp, D. J. Three microtubule severing enzymes contribute to the Pacman-flux machinery that moves chromosomes. The Journal of cell biology 177, 231-242 (2007
17. Hartman, J. J., et al. Katanin, A microtubule-severing protein, is A novel AAA ATPase that targets to the centrosome using A WD40-containing subunit. Cell 93, 277-287 (1998
18. Hu, W. F., et al. Katanin p80 regulates human cortical development by limiting centriole and cilia number. Neuron 84, 1240-1257 (2014
19. Mishra-Gorur, K., et al. Mutations in KATNB1 cause complex cerebral malformations by disrupting asymmetrically dividing neural progenitors. Neuron 84, 1226-1239 (2014
20. Kardon, J. R., & Vale, R. D. Regulators of the cytoplasmic dynein motor. Nature reviews. Molecular cell biology 10, 854-865 (2009
21. Lydersen, B. K., & Pettijohn, D. E. Human-specific nuclear protein that associates with the polar region of the mitotic apparatus: distribution in A human/hamster hybrid cell. Cell 22, 489-499 (1980
22. Radulescu, A. E., & Cleveland, D. W. NuMA after 30 years: the matrix revisited. Trends in cell biology 20, 214-222 (2010
23. Toyo-Oka, K., et al. Recruitment of katanin p60 by phosphorylated NDEL1, an LIS1 interacting protein, is essential for mitotic cell division and neuronal migration. Human molecular genetics 14, 3113-3128 (2005
24. Cheung, K., et al. Proteomic Analysis of the Mammalian Katanin Family of Microtubule-severing Enzymes Defines Katanin p80 subunit B-like 1 (KATNBL1) as A Regulator of Mammalian Katanin Microtubule-severing. Molecular & cellular proteomics: MCP 15, 1658-1669 (2016
25. Yamada, M., et al. LIS1 and NDEL1 coordinate the plus-end-directed transport of cytoplasmic dynein. The EMBO journal 27, 2471-2483 (2008
26. Tsai, L. H., & Gleeson, J. G. Nucleokinesis in neuronal migration. Neuron 46, 383-388 (2005
27. Yang, C. H., & Snyder, M. The nuclear-mitotic apparatus protein is important in the establishment and maintenance of the bipolar mitotic spindle apparatus. Molecular biology of the cell 3, 1259-1267 (1992
28. Galderisi, U., Jori, F. P., & Giordano, A. Cell cycle regulation and neural differentiation. Oncogene 22, 5208-5219 (2003
29. Lancaster, M. A., et al. Cerebral organoids model human brain development and microcephaly. Nature 501, 373-379 (2013
30. Mochida, G. H. Genetics and biology of microcephaly and lissencephaly. Seminars in pediatric neurology 16, 120-126 (2009
31. McNally, K. P., Bazirgan, O. A., & McNally, F. J. Two domains of p80 katanin regulate microtubule severing and spindle pole targeting by p60 katanin. Journal of cell science 113 (Pt 9), 1623-1633 (2000
32. Kuijpers, M., & Hoogenraad, C. C. Centrosomes, microtubules and neuronal development. Molecular and cellular neurosciences 48, 349-358 (2011
33. Sakakibara, A., et al. Dynamics of centrosome translocation and microtubule organization in neocortical neurons during distinct modes of polarization. Cerebral cortex 24, 1301-1310 (2014
34. Tanaka, T., et al. Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. The Journal of cell biology 165, 709-721 (2004
35. Nadarajah, B., Brunstrom, J. E., Grutzendler, J., Wong, R. O., & Pearlman, A. L. Two modes of radial migration in early development of the cerebral cortex. Nature neuroscience 4, 143-150 (2001
36. Noctor, S. C., Martinez-Cerdeno, V., Ivic, L., & Kriegstein, A. R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nature neuroscience 7, 136-144 (2004
37. Tabata, H., & Nakajima, K. Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. The Journal of neuroscience: the official journal of the Society for Neuroscience 23, 9996-10001 (2003
38. Gaglio, T., Saredi, A., & Compton, D. A. NuMA is required for the organization of microtubules into aster-like mitotic arrays. The Journal of cell biology 131, 693-708 (1995
39. Merdes, A., Ramyar, K., Vechio, J. D., & Cleveland, D. W. A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell 87, 447-458 (1996
40. Poulson, N. D., & Lechler, T. Asymmetric cell divisions in the epidermis. International review of cell and molecular biology 295, 199-232 (2012
41. Qi, R., et al. The lamin-A/C-LAP2alpha-BAF1 protein complex regulates mitotic spindle assembly and positioning. Journal of cell science 128, 2830-2841 (2015
42. Ferhat, L., Cook, C., Kuriyama, R., & Baas, P. W. The nuclear/mitotic apparatus protein NuMA is A component of the somatodendritic microtubule arrays of the neuron. Journal of neurocytology 27, 887-899 (1998
43. Tang, T. K., Tang, C. J., Chao, Y. J., & Wu, C. W. Nuclear mitotic apparatus protein (NuMA): spindle association, nuclear targeting and differential subcellular localization of various NuMA isoforms. Journal of cell science 107 (Pt 6), 1389-1402 (1994
44. Harborth, J., Wang, J., Gueth-Hallonet, C., Weber, K., & Osborn, M. Self assembly of NuMA: multiarm oligomers as structural units of A nuclear lattice. The EMBO journal 18, 1689-1700 (1999
45. Jin, M., Yamada, M., Arai, Y., Nagai, T., & Hirotsune, S. Arl3 and LC8 regulate dissociation of dynactin from dynein. Nature communications 5, 5295 (2014
46. Tabata, H., & Nakajima, K. Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103, 865-872 (2001