Activation of Aurora-A is essential for neuronal migration via modulation of microtubule organization

Journal of Neuroscience

Volumn 32, Issue 32, 2012, Pages 11050-11066

  Takitoh, Takako ^a   Kumamoto, Kanako ^a   Wang, Chen Chi ^b,c   Sato, Makoto ^b,c   Toba, Shiori ^a   Wynshaw Boris, Anthony ^d   Hirotsune, Shinji ^a  

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

^b UNIVERSITY OF FUKUI   (Japan)

^c UNIVERSITY OF FUKUI   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA A KINASE; CYCLIN DEPENDENT KINASE 5; CYTOSKELETON PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; PROTEIN NDEL 1; RAP PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; FEMALE; HISTOLOGY; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MALE; MICROTUBULE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

AMIODARONE; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BROMODEOXYURIDINE; CALCIUM-BINDING PROTEINS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL MOVEMENT; CELLS, CULTURED; CEREBELLUM; CYCLIN-DEPENDENT KINASE 5; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MUTATION; NEURONS; PHOSPHORYLATION; PIPERAZINES; PREGNANCY; PROTEIN-SERINE-THREONINE KINASES; PURINES; RNA, SMALL INTERFERING; SEX FACTORS; SIGNAL TRANSDUCTION;

EID: 84864859065     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5664-11.2012     Document Type: Article

References (51)

1. Aliagas-Martin I, Burdick D, Corson L, Dotson J, Drummond J, Fields C, Huang OW, Hunsaker T, Kleinheinz T, Krueger E, Liang J, Moffat J, Phillips G, Pulk R, Rawson TE, Ultsch M, Walker L, Wiesmann C, Zhang B, Zhu BY, et al. (2009) A class of 2,4-bisanilinopyrimidine Aurora A inhibitors with unusually high selectivity against Aurora B. J Med Chem 52:3300-3307.
2. Azimzadeh J, Bornens M (2007) Structure and duplication of the centrosome. J Cell Sci 120:2139-2142.
3. Bettencourt-Dias M, Glover DM (2007) Centrosome biogenesis and function: centrosomics brings new understanding. Nat Rev Mol Cell Biol 8:451-463.
4. Bond J, Roberts E, Springell K, Lizarraga SB, Scott S, Higgins J, Hampshire DJ, Morrison EE, Leal GF, Silva EO, Costa SM, Baralle D, Raponi M, Karbani G, Rashid Y, Jafri H, Bennett C, Corry P, Walsh CA, Woods CG (2005) A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat Genet 37:353-355.
5. Buchman JJ, Tseng HC, Zhou Y, Frank CL, Xie Z, Tsai LH (2010) Cdk5rap2 interacts with pericentrin to maintain the neural progenitor pool in the developing neocortex. Neuron 66:386-402.
6. Burkhardt JK, Echeverri CJ, Nilsson T, Vallee RB (1997) Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dyneindependent maintenance of membrane organelle distribution. J Cell Biol 139:469-484.
7. Choi YK, Liu P, Sze SK, Dai C, Qi RZ (2010) CDK5RAP2 stimulates microtubule nucleation by the gamma-tubulin ring complex. J Cell Biol 191:1089-1095.
8. Dhavan R, Tsai LH (2001) A decade of CDK5. Nat Rev Mol Cell Biol 2:749-759.
9. Distel M, Hocking JC, Volkmann K, Köster RW (2010) The centrosome neither persistently leads migration nor determines the site of axonogenesis in migrating neurons in vivo. J Cell Biol 191:875-890.
10. Doxsey S, Zimmerman W, Mikule K (2005) Centrosome control of the cell cycle. Trends Cell Biol 15:303-311.
11. Giet R, Uzbekov R, Cubizolles F, Le Guellec K, Prigent C (1999) The Xenopus laevis Aurora-related protein kinase pEg2 associates with and phosphorylates the kinesin-related protein XlEg5. J Biol Chem 274:15005-15013.
12. Giet R, McLean D, Descamps S, Lee MJ, Raff JW, Prigent C, Glover DM (2002) Drosophila Aurora A kinase is required to localize D-TACC to centrosomes and to regulate astral microtubules. J Cell Biol 156:437-451.
13. Glover DM, Leibowitz MH, McLean DA, Parry H (1995) Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles. Cell 81:95-105.
14. Gupta A, Tsai LH (2003) Cyclin-dependent kinase 5 and neuronal migration in the neocortex. Neurosignals 12:173-179.
15. Harrington EA, Bebbington D, Moore J, Rasmussen RK, Ajose-Adeogun AO, Nakayama T, Graham JA, Demur C, Hercend T, Diu-Hercend A, Su M, Golec JM, Miller KM (2004) VX-680, a potent and selective smallmolecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nat Med 10:262-267.
16. Hatten ME (1985) Neuronal regulation of astroglial morphology and proliferation in vitro. J Cell Biol 100:384-396.
17. Hatten ME (1999) Central nervous system neuronal migration. Annu Rev Neurosci 22:511-539.
18. Hebbar S, Mesngon MT, Guillotte AM, Desai B, Ayala R, Smith DS (2008) Lis1 and Ndel1 influence the timing of nuclear envelope breakdown in neural stem cells. J Cell Biol 182:1063-1071.
19. Higginbotham HR, Gleeson JG (2007) The centrosome in neuronal development. Trends Neurosci 30:276-283.
20. Krystyniak A, Garcia-Echeverria C, Prigent C, Ferrari S (2006) Inhibition of Aurora A in response to DNA damage. Oncogene 25:338-348.
21. Kufer TA, Silljé HH, Körner R, Gruss OJ, Meraldi P, Nigg EA (2002) Human TPX2 is required for targeting Aurora-A kinase to the spindle. J Cell Biol 158:617-623.
22. Lizarraga SB, Margossian SP, Harris MH, Campagna DR, Han AP, Blevins S, Mudbhary R, Barker JE, Walsh CA, Fleming MD (2010) Cdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors. Development 137:1907-1917.
23. Malumbres M (2011) Physiological relevance of cell cycle kinases. Physiol Rev 91:973-1007.
24. Megraw TL, Sharkey JT, Nowakowski RS (2011) Cdk5rap2 exposes the centrosomal root of microcephaly syndromes. Trends Cell Biol 21:470-480.
25. Mimori-Kiyosue Y, Shiina N, Tsukita S (2000) The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules. Curr Biol 10:865-868.
26. Mori D, Yano Y, Toyo-oka K, Yoshida N, Yamada M, Muramatsu M, Zhang D, Saya H, Toyoshima YY, Kinoshita K, Wynshaw-Boris A, Hirotsune S (2007) NDEL1 phosphorylation by Aurora-A kinase is essential for centrosomal maturation, separation, and TACC3 recruitment. Mol Cell Biol 27:352-367.
27. Mori D, Yamada M, Mimori-Kiyosue Y, Shirai Y, Suzuki A, Ohno S, Saya H, Wynshaw-Boris A, Hirotsune S (2009) An essential role of the aPKCAurora A-NDEL1 pathway in neurite elongation by modulation of microtubule dynamics. Nat Cell Biol 11:1057-1068.
28. Niethammer M, Smith DS, Ayala R, Peng J, Ko J, Lee MS, Morabito M, Tsai LH (2000) NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 28:697-711.
29. Nigg EA (2001) Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2:21-32.
30. Nigg EA, Raff JW (2009) Centrioles, centrosomes, and cilia in health and disease. Cell 139:663-678.
31. Patrick GN, Zhou P, Kwon YT, Howley PM, Tsai LH (1998) p35, the neuronalspecific activator of cyclin-dependent kinase 5 (Cdk5) is degraded by the ubiquitin-proteasome pathway. J Biol Chem 273:24057-24064.
32. Pugacheva EN, Jablonski SA, Hartman TR, Henske EP, Golemis EA (2007) HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 129:1351-1363.
33. Saito T, Nakatsuji N (2001) Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev Biol 240:237-246.
34. Sasaki S, Shionoya A, Ishida M, Gambello MJ, Yingling J, Wynshaw-Boris A, Hirotsune S (2000) A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 28:681-696.
35. Sasaki S, Mori D, Toyo-oka K, Chen A, Garrett-Beal L, Muramatsu M, Miyagawa S, Hiraiwa N, Yoshiki A, Wynshaw-Boris A, Hirotsune S (2005) Complete loss of Ndel1 results in neuronal migration defects and early embryonic lethality. Mol Cell Biol 25:7812-7827.
36. Sauer ME, Walker BE (1959) Radioautographic study of interkinetic nuclear migration in the neural tube. Proc Soc Exp Biol Med 101:557-560.
37. Sidman RL, Rakic P (1973) Neuronal migration, with special reference to developing human brain: a review. Brain Res 62:1-35.
38. Su SC, Tsai LH (2011) Cyclin-dependent kinases in brain development and disease. Annu Rev Cell Dev Biol 27:465-491.
39. Tabata H, Nakajima K (2001) 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.
40. Terada Y, Uetake Y, Kuriyama R (2003) Interaction of Aurora-A and centrosomin at the microtubule-nucleating site in Drosophila and mammalian cells. J Cell Biol 162:757-763.
41. Torisawa T, Nakayama A, Furuta K, Yamada M, Hirotsune S, Toyoshima YY (2011) Functional dissection of LIS1 and NDEL1 towards understanding the molecular mechanisms of cytoplasmic dynein regulation. J Biol Chem 286:1959-1965.
42. Toyo-Oka K, Sasaki S, Yano Y, Mori D, Kobayashi T, Toyoshima YY, Tokuoka SM, Ishii S, Shimizu T, Muramatsu M, Hiraiwa N, Yoshiki A, Wynshaw-Boris A, Hirotsune S (2005) Recruitment of katanin p60 by phosphorylated NDEL1, an LIS1 interacting protein, is essential for mitotic cell division and neuronal migration. Hum Mol Genet 14:3113-3128.
43. Tsai LH, Gleeson JG (2005) Nucleokinesis in neuronal migration. Neuron 46:383-388.
44. Van Horn RD, Chu S, Fan L, Yin T, Du J, Beckmann R, Mader M, Zhu G, Toth J, Blanchard K, Ye XS (2010) Cdk1 activity is required for mitotic activation of Aurora A during G2/M transition of human cells. J Biol Chem 285:21849-21857.
45. Wang CX, Song JH, Song DK, Yong VW, Shuaib A, Hao C (2006) Cyclindependent kinase-5 prevents neuronal apoptosis through ERK-mediated upregulation of Bcl-2. Cell Death Differ 13:1203-1212.
46. Wang X, Ching YP, Lam WH, Qi Z, Zhang M, Wang JH (2000) Identification of a common protein association region in the neuronal Cdk5 activator. J Biol Chem 275:31763-31769.
47. Yamada M, Toba S, Yoshida Y, Haratani K, Mori D, Yano Y, Mimori-Kiyosue Y, Nakamura T, Itoh K, Fushiki S, Setou M, Wynshaw-Boris A, Torisawa T, Toyoshima YY, Hirotsune S (2008) LIS1 and NDEL1 coordinate the plusend- directed transport of cytoplasmic dynein. EMBO J 27:2471-2483.
48. Yamada M, Yoshida Y, Mori D, Takitoh T, Kengaku M, Umeshima H, Takao K, Miyakawa T, Sato M, Sorimachi H, Wynshaw-Boris A, Hirotsune S (2009) Inhibition of calpain increases LIS1 expression and partially rescues in vivo phenotypes in a mouse model of lissencephaly. Nat Med 15:1202-1207.
49. Yamada M, Toba S, Takitoh T, Yoshida Y, Mori D, Nakamura T, Iwane AH, Yanagida T, Imai H, Yu-Lee LY, Schroer T, Wynshaw-Boris A, Hirotsune S (2010) mNUDC is required for plus-end-directed transport of cytoplasmic dynein and dynactins by kinesin-1. EMBO J 29:517-531.
50. Yan X, Li F, Liang Y, Shen Y, Zhao X, Huang Q, Zhu X (2003) Human Nudel and NudE as regulators of cytoplasmic dynein in poleward protein transport along the mitotic spindle. Mol Cell Biol 23:1239-1250.
51. Zylkiewicz E, Kijanska M, Choi WC, Derewenda U, Derewenda ZS, Stukenberg PT (2011) The N-terminal coiled-coil of Ndel1 is a regulated scaffold that recruits LIS1 to dynein. J Cell Biol 192:433-445.