Novel embryonic neuronal migration and proliferation defects in Dcx mutant mice are exacerbated by Lis1 reduction

Journal of Neuroscience

Volumn 30, Issue 8, 2010, Pages 3002-3012

  Pramparo, Tiziano ^a   Youn, Yong Ha ^a   Yingling, Jessica ^b   Hirotsune, Shinji ^c   Wynshaw Boris, Anthony ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; FEMALE; GENE INTERACTION; GLIA CELL; HIPPOCAMPUS; MALE; NEOCORTEX; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

1-ALKYL-2-ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; ANIMALS; BRAIN; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SHAPE; CELLS, CULTURED; CEREBRAL CORTEX; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; NERVOUS SYSTEM MALFORMATIONS; NEUROGENESIS; NEUROGLIA; NEURONS; NEUROPEPTIDES; ORGAN CULTURE TECHNIQUES; SPHEROIDS, CELLULAR; STEM CELLS;

EID: 77649134493     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4851-09.2010     Document Type: Article

References (44)

1. Bai J, Ramos RL, Ackman JB, Thomas AM, Lee RV, LoTurco JJ (2003) RNAi reveals doublecortin is required for radial migration in rat neocortex. Nat Neurosci 6:1277-1283.
2. Bantubungi K, Blum D, Cuvelier L, Wislet-Gendebien S, Rogister B, Brouillet E, Schiffmann SN (2008) Stem cell factor and mesenchymal and neural stem cell transplantation in a rat model of Huntington's disease. Mol Cell Neurosci 37:454-470.
3. Brown JP, Couillard-Després S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
4. Caspi M, Atlas R, Kantor A, Sapir T, Reiner O (2000) Interaction between LIS1 and doublecortin, two lissencephaly gene products. Hum Mol Genet 9:2205-2213.
5. Corbo JC, Deuel TA, Long JM, LaPorte P, Tsai E, Wynshaw-Boris A, Walsh CA (2002) Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J Neurosci 22:7548-7557.
6. des Portes V, Pinard JM, Billuart P, Vinet MC, Koulakoff A, Carrié A, Gelot A, Dupuis E, Motte J, Berwald-Netter Y, Catala M, Kahn A, Beldjord C, Chelly J (1998) A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92:51-61.
7. Dobyns WB, Reiner O, Carrozzo R, Ledbetter DH (1993) Lissencephaly. A human brain malformation associated with deletion of the LIS1 gene located at chromosome 17p13. JAMA 270:2838-2842.
8. Feng Y, Walsh CA (2004) Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44:279-293.
9. Friocourt G, Liu JS, Antypa M, Rakic S, Walsh CA, Parnavelas JG (2007) Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J Neurosci 27:3875-3883.
10. Gambello MJ, Darling DL, Yingling J, Tanaka T, Gleeson JG, Wynshaw-Boris A (2003) Multiple dose-dependent effects of Lis1 on cerebral cortical development. J Neurosci 23:1719-1729.
11. Gleeson JG, Allen KM, Fox JW, Lamperti ED, Berkovic S, Scheffer I, Cooper EC, Dobyns WB, Minnerath SR, Ross ME, Walsh CA (1998) Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92:63-72.
12. Gleeson JG, Lin PT, Flanagan LA, Walsh CA (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257-271.
13. Gönczy P, Bellanger JM, Kirkham M, Pozniakowski A, Baumer K, Phillips JB, Hyman AA (2001) zyg-8, a gene required for spindle positioning in C. elegans, encodes a doublecortin-related kinase that promotes microtubule assembly. Dev Cell 1:363-375.
14. Götz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777-788.
15. Guerrini R, Dobyns WB, Barkovich AJ (2008) Abnormal development of the human cerebral cortex: genetics, functional consequences and treatment options. Trends Neurosci 31:154-162.
16. Gupta A, Tsai LH, Wynshaw-Boris A (2002) Life is a journey: a genetic look at neocortical development. Nat Rev Genet 3:342-355.
17. Hirotsune S, Fleck MW, Gambello MJ, Bix GJ, Chen A, Clark GD, Ledbetter DH, McBain CJ, Wynshaw-Boris A (1998) Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat Genet 19:333-339.
18. Ishii Y, Matsumoto Y, Watanabe R, Elmi M, Fujimori T, Nissen J, Cao Y, Nabeshima Y, Sasahara M, Funa K (2008) Characterization of neuroprogenitor cells expressing the PDGF beta-receptor within the subventricular zone of postnatal mice. Mol Cell Neurosci 37:507-518.
19. Kappeler C, Saillour Y, Baudoin JP, Tuy FP, Alvarez C, Houbron C, Gaspar P, Hamard G, Chelly J, Métin C, Francis F (2006) Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice. Hum Mol Genet 15:1387-1400.
20. Kato M, Dobyns WB (2003) Lissencephaly and the molecular basis of neuronal migration. Hum Mol Genet 12 (Spec No 1):R89-R96.
21. Kerjan G, Koizumi H, Han EB, Dubé CM, Djakovic SN, Patrick GN, Baram TZ, Heinemann SF, Gleeson JG (2009) Mice lacking doublecortin and doublecortin-like kinase 2 display altered hippocampal neuronal maturation and spontaneous seizures. Proc Natl Acad Sci U S A 106:6766-6771.
22. Koizumi H, Higginbotham H, Poon T, Tanaka T, Brinkman BC, Gleeson JG (2006a) Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain. Nat Neurosci 9:779-786.
23. Koizumi H, Tanaka T, Gleeson JG (2006b) Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 49:55-66.
24. Kosodo Y, Röper K, Haubensak W, Marzesco AM, Corbeil D, Huttner WB (2004) Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J 23:2314-2324.
25. Learish RD, Bruss MD, Haak-Frendscho M (2000) Inhibition of mitogen-activated protein kinase kinase blocks proliferation of neural progenitor cells. Brain Res Dev Brain Res 122:97-109.
26. Lo Nigro C, Chong CS, Smith AC, Dobyns WB, Carrozzo R, Ledbetter DH (1997) Point mutations and an intragenic deletion in LIS1, the lissencephaly causative gene in isolated lissencephaly sequence and Miller-Dieker syndrome. Hum Mol Genet 6:157-164.
27. Matsumoto N, Leventer RJ, Kuc JA, Mewborn SK, Dudlicek LL, Ramocki MB, Pilz DT, Mills PL, Das S, Ross ME, Ledbetter DH, Dobyns WB (2001) Mutation analysis of the DCX gene and genotype/phenotype correlation in subcortical band heterotopia. Eur J Hum Genet 9:5-12.
28. McManus MF, Nasrallah IM, Pancoast MM, Wynshaw-Boris A, Golden JA (2004) Lis1 is necessary for normal non-radial migration of inhibitory interneurons. Am J Pathol 165:775-784.
29. Nadarajah B, Brunstrom JE, Grutzendler J, Wong RO, Pearlman AL (2001) Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci 4:143-150.
30. 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.
31. Ramos RL, Bai J, LoTurco JJ (2006) Heterotopia formation in rat but not mouse neocortex after RNA interference knockdown of DCX. Cereb Cortex 16:1323-1331.
32. Reiner O, Carrozzo R, Shen Y, Wehnert M, Faustinella F, Dobyns WB, Caskey CT, Ledbetter DH (1993) Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 364:717-721.
33. Reynolds BA, Tetzlaff W, Weiss S (1992) A multipotent EGF responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12:4565-4574.
34. Rietze RL, Reynolds BA (2006) Neural stem cell isolation and characterization. Methods Enzymol 419:3-23.
35. 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.
36. Shu T, Tseng HC, Sapir T, Stern P, Zhou Y, Sanada K, Fischer A, Coquelle FM, Reiner O, Tsai LH (2006) Doublecortin-like kinase controls neurogenesis by regulating mitotic spindles and M phase progression. Neuron 49:25-39.
37. Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG (2004) Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 165:709-721.
38. Toyo-oka K, Shionoya A, Gambello MJ, Cardoso C, Leventer R, Ward HL, Ayala R, Tsai LH, Dobyns W, Ledbetter D, Hirotsune S, Wynshaw-Boris A (2003) 14-3-3epsilon is important for neuronal migration by binding to NUDEL: a molecular explanation for Miller-Dieker syndrome. Nat Genet 34:274-285.
39. Vallee RB, Tsai JW (2006) The cellular roles of the lissencephaly gene LIS1, and what they tell us about brain development. Genes Dev 20:1384-1393.
40. Vreugdenhil E, Kolk SM, Boekhoorn K, Fitzsimons CP, Schaaf M, Schouten T, Sarabdjitsingh A, Sibug R, Lucassen PJ (2007) Doublecortin-like, a microtubule-associated protein expressed in radial glia, is crucial for neuronal precursor division and radial process stability. Eur J Neurosci 25:635-648.
41. Walker TL, Yasuda T, Adams DJ, Bartlett PF (2007) The doublecortin-expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells. J Neurosci 27:3734-3742.
42. Wynshaw-Boris A (2007) Lissencephaly and LIS1: insights into the molecular mechanisms of neuronal migration and development. Clin Genet 72:296-304.
43. Yingling J, Youn YH, Darling D, Toyo-Oka K, Pramparo T, Hirotsune S, Wynshaw-Boris A (2008) Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 132:474-486.
44. Youn YH, Pramparo T, Hirotsune S, Wynshaw-Boris A (2009) Distinct dose-dependent cortical neuronal migration and neurite extension defects in Lis1 and Ndel1 mutant mice. J Neurosci 29:15520-15530.