Protein-protein interactions, cytoskeletal regulation and neuronal migration

Nature Reviews Neuroscience

Volumn 2, Issue 6, 2001, Pages 408-416

  Feng, Yuanyi ^a   Walsh, Christopher A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA;

1 ALKYL 2 ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; CYTOSKELETON PROTEIN; DOUBLECORTIN PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NEUROPEPTIDE; PAFAH1B1 PROTEIN, HUMAN;

ANIMAL; BRAIN; CELL MOTION; CELL SIZE; CONGENITAL MALFORMATION; GENETICS; HUMAN; METABOLISM; NERVOUS SYSTEM MALFORMATION; PATHOPHYSIOLOGY; REVIEW;

1-ALKYL-2-ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; ANIMALS; BRAIN; CELL MOVEMENT; CELL SIZE; CYTOSKELETAL PROTEINS; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; NERVOUS SYSTEM MALFORMATIONS; NEUROPEPTIDES;

EID: 0035374379     PISSN: 14710048     EISSN: None     Source Type: Journal    
DOI: 10.1038/35077559     Document Type: Review

References (77)

1. Jellinger, K. & Rett, A. Agyria-pachygyria (lissencephaly syndrome). Neuropadiatrie 7, 66-91 (1976).
2. Alvarez, L. A. et al. Miller-Dieker syndrome: a disorder affecting specific pathways of neuronal migration. Neurology 36, 489-493 (1986).
3. Kuchelmeister, K., Bergmann, M. & Gullotta, F. Neuropathology of lissencephalies. Childs Nerv. Syst. 9, 394-399 (1993).
4. Rakic, P. Neuronal migration and contact guidance in the primate telencephalon. Postgrad. Med. J. 54, 25-40 (1978).
5. Gleeson, J. G. & Walsh, C. A. Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci. 23, 352-359 (2000).
6. Dobyns, W. B., Reiner, O., Carrozzo, R. & Ledbetter, D. H. Lissencephaly: a human brain malformation associated with deletion of the LIS1 gene located at chromosome 17p13. J. Am. Med. Assoc. 270, 2838-2842 (1993).
7. Lo Nigro, C. et al. 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 (1997).
8. Reiner, O. et al. Isolation of a Miller-Dieker lissencephaly gene containing G protein β-subunit-like repeats. Nature 364, 717-721 (1993).
9. Hirotsune, S. et al. Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nature Genet. 19, 333-339 (1998).
10. des Portes, V. et al. Doublecortin is the major gene causing X-linked subcortical laminar heterotopia (SCLH). Hum. Mol. Genet. 7, 1063-1070 (1998).
11. 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).
12. Gleeson, J. G., Lin, P. T., Flanagan, L. A. & Walsh, C. A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23, 257-271 (1999).
13. Francis, F. et al. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23, 247-256 (1999).
14. Horesh, D. et al. Doublecortin, a stabilizer of microtubules. Hum. Mol. Genet. 8, 1599-1610 (1999). References 12-14 describe the functional characterization of DCX protein as a MAP, and suggest that DCX functions in neuronal migration by stabilizing microtubules.
15. Geyer, M. & Wittinghofer, A. GEFs, GAPs, GDIs and effectors: taking a closer (3D) look at the regulation of Ras-related GTP-binding proteins. Curr. Opin. Struct. Biol. 7, 786-792 (1997).
16. Nassar, N. et al. The 2. 2 A crystal structure of the Ras-binding domain of the serine/threonine kinase c-Raf1 in complex with Rap1A and a GTP analogue. Nature 375, 554-560 (1995).
17. Taylor, K. R., Holzer, A. K., Bazan, J. F., Walsh, C. A. & Gleeson, J. G. Patient mutations in doublecortin define a repeated tubulin-binding domain. J. Biol. Chem. 275, 34442-34450 (2000).
18. Drechsel, D. N., Hyman, A. A., Cobb, M. H. & Kirschner, M. W. Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol. Biol. Cell 3, 1141-1154 (1992).
19. Kaech, S., Ludin, B. & Matus. A. Cytoskeletal plasticity in cells expressing neuronal microtubule-associated proteins. Neuron 17, 1189-1199 (1996).
20. Garner, C. C., Garner, A., Huber, G., Kozak, C. & Matus, A. Molecular cloning of microtubule-associated protein 1 (MAP1A) and microtubule-associated protein 5 (MAP1B): identification of distinct genes and their differential expression in developing brain. J. Neurochem. 55, 146-154 (1990).
21. Schoenfeld, T. A., McKerracher, L., Obar, R. & Vallee, R. B. MAP 1A and MAP 1B are structuraly related microtubule associated proteins with distinct developmental patterns in the CNS. J. Neurosci. 9, 1712-1730 (1989).
22. Chen, J., Kanai, Y., Cowan, N. J. & Hirokawa, N. Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature 360, 674-677 (1992).
23. Sapir, T. et al. Doublecortin mutations cluster in evolutionarily conserved functional domains. Hum. Mol. Genet. 9, 703-712 (2000).
24. Rakic, P., Knyihar-Csillik, E. & Csillik, B. Polarity of microtubule assemblies during neuronal cell migration. Proc. Natl Acad. Sci. USA 93, 9218-9222 (1996).
25. Lin, P. T., Gleeson, J. G., Corbo, J. C., Flanagan, L. & Walsh, C. A. DCAMKL1 encodes a protein kinase with homology to doublecortin that regulates microtubule polymerization. J. Neurosci. 20, 9152-9161 (2000).
26. Burgess, H. A. & Reiner, O. Doublecortin-like kinase is associated with microtubules in neuronal growth cones. Mol. Cell. Neurosci. 16, 529-541 (2000).
27. Garcia-Higuera, I. et al. Folding of proteins with WD-repeats: comparison of six members of the WD-repeat superfamily to the G protein β subunit. Biochemistry 35, 13985-13994 (1996).
28. Hattori, M., Adachi, H., Tsujimoto, M., Arai, H. & Inoue, K. Miller-Dieker lissencephaly gene encodes a subunit of brain platelet-activating factor acetylhydrolase. Nature 370, 216-218 (1994).
29. Brunati, A. M. et al. The spleen protein-tyrosine kinase TPK-IIB is highly similar to the catalytic domain of p72syk. Eur. J. Biochem. 240, 400-407 (1996).
30. Kurosaki, T. Molecular dissection of B cell antigen receptor signaling (review). Int. J. Mol. Med. 1, 515-527 (1998).
31. Sapir, T., Elbaum, M. & Reiner, O. Reduction of microtubule catastrophe events by LIS1, platelet-activating factor acetylhydrolase subunit. EMBO J. 16, 6977-6984 (1997). Presented the observation of the colocalization of LIS1 with the microtubule network, its direct binding to polymerized microtubules and its activity in reducing microtubule catastrophe events in vitro.
32. Oakley, B. R. & Morris, N. R. Nuclear movement is β-tubulin-dependent in Aspergillus nidulans. Cell 19, 255-262 (1980).
33. Morris, N. R., Lai, M. H. & Oakley, C. E. Identification of a gene for α-tubulin in Aspergillus nidulans. Cell 16, 437-442 (1979).
34. Oakley, C. E. & Oakley, B. R. Identification of γ-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature 338, 662-664 (1989).
35. Xiang, X. Roghi, C. & Morris, N. R. Characterization and localization of the cytoplasmic dynein heavy chain in Aspergillus nidulans. Proc. Natl Acad. Sci. USA 92, 9890-9894 (1995).
36. Robb, M. J., Wilson, M. A. & Vierula, P. J. A fungal actin-related protein involved in nuclear migration. Mol. Gen. Genet. 247, 583-590 (1995).
37. Xiang, X. Osmani, A. H., Osmani, S. A., Xin, M. & Morris, N. R. NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol. Biol. Cell 6, 297-310 (1995).
38. Wins, D. A., Liu, B., Xiang, X. & Morris, N. R. Mutations in the heavy chain of cytoplasmic dynein suppress the nudF nuclear migration mutation of Aspergillus nidulans. Mol. Gen. Genet. 255, 194-200 (1997).
39. Willins, D. A., Xiang, X. & Morris, N. R. An α tubulin mutation suppresses nuclear migration mutations in Aspergillus nidulans. Genetics 141, 1287-1298 (1995).
40. Efimov, V. P. & Morris, N. R. The LIS1-related NUDF protein of Aspergillus nidulans interacts with the coiled-coil domain of the NUDE/RO11 protein. J. Cell Biol. 150, 681-683 (2000).
41. Feng, Y. et al. LIS1 regulates CNS lamination by interacting with mNudE, a central component of the centrosome. Neuron 28, 665-679 (2000). Describes the functional characterization of mNudE and LIS1-NUDE interactions. Showed that mNudE is a potential central scaffold of the microtubule-organizing centre, and that LISI-NUDE interactions are required for the lamination of anterior CNS structures in Xenopus embryos.
42. Sasaki, S. et al. A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 28, 681-696 (2000). Presented evidence that LIS1 and NUDEL form complexes with dynein in the mammalian CNS, and that LIS1 and NUDEL regulate the cellular localization of dynein. It also showed that NUDEL is an in vitro substrate of Cdk5.
43. Niethammer, M. et al. NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 28, 697-711 (2000). Demonstrated that NUDEL interacts with cytoplasmic dynein, and is a phosphoprotein in mammalian brain and a substrate of CdK5. The distribution of NUDEL is regulated by Cdk5 activity.
44. Kitagawa, M. et al. Direct association of LIS1, the lissencephaly gene product, with a mammalian homologue of a fungal nuclear distribution protein, rNUDE. FEBS Lett. 479, 57-62 (2000).
45. Sweeney, K. J., Prokscha, A. & Eichele, G. NudE-L, a novel Lis1-interacting protein, belongs to a family of vertebrate coiled-coil proteins. Mech. Dev. 101, 21-33 (2001).
46. Faulkner, N. E. et al. A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nature Cell Biol. 2, 784-791 (2000). Demonstrated that LIS1 interacts with dynein and dynactin, and that overexpression of LIS1 in cultured mammalian cells interferes with mitotic progression and leads to spindle misorientation. Suggests that a LIS1-dynein interaction regulates cell division.
47. Smith, D. S. et al. Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian Lis1. Nature Cell Biol. 2, 767-775 (2000). Identified that LIS1 forms complexes with cytoplasmic dynein/dynactin, and presented experimental evidence suggesting that LIS1 regulates cytoplasmic dynein distribution.
48. Liu, Z., Xie, T. & Steward, R. Lis1, the Drosophila homolog of a human lissencephaly disease gene, is required for germline cell division and occyte differentiation. Development 126, 4477-4488 (1999).
49. Swan, A., Nguyen, T. & Suter, B. Drosophila Lissencephaly-1 functions with Bic-D and dynein in occyte determination and nuclear positioning. Nature Cell Biol. 1, 444-449 (1999).
50. Liu, Z., Steward, R. & Luo, L. Drosophila Lis1 is required for neuroblast proliferation, dendritic elaboration and axonal transport. Nature Cell Bol. 2, 776-783 (2000). By a mosaic analysis using a Lis1 null mutation, this paper showed that Lis1 is required for neuroblast proliferation and axonal transport It also showed that neurons containing a mutated cytoplasmic dynein heavy chain (Dhc64C) exhibit pnenotypes similar to Lis1 mutants.
51. 2+ fluctuations modulate the rate of neuronal migration. Neuron 17, 275-285 (1996).
52. Hatten, M. E. Central nervous system neuronal migration. Annu. Rev. Neurosci. 22, 511-539 (1999).
53. Rivas, R. J. & Hatten, M. E. Motility and cytoskeletal organization of migrating cerebellar granule neurons. J. Neurosci. 15, 981-989 (1995).
54. 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 Neurosci. 4, 143-150 (2001).
55. Caspi, M., Atlas, R., Kantor, A., Sapir, T. & Reiner, O. Interaction between LIS1 and doublecortin, two lissencephaly gene products. Hum. Mol. Genet. 9, 2205-2213 (2000).
56. Sapir, T., Cahana, A., Seger, R., Nekhai, S. & Reiner, O. LIS1 is a microtubule-associated phosphoprotein. Eur. J. Biochem. 265, 181-188 (1999).
57. Peters, J. D., Furlong, M. T., Asai, D. J., Harrison, M. L. & Geahlen, R. L. Syk, activated by cross-linking the B-cell antigen receptor, localizes to the cytosd where it interacts with and phosphorylates α-tubulin on tyrosine. J. Biol. Chem. 271, 4755-4762 (1996).
58. Faruki, S., Geahlen, R. L. & Asai, D. J. Syk-dependent phosphorylation of microtubules in activated B-lymphocytes. J. Cell Sci. 113, 2557-2565 (2000).
59. Stukenberg, P. T. et al. Systematic identification of mitotic phosphoproteins. Curr. Biol. 7, 338-348 (1997).
60. Ohshima, T. et al. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl Acad. Sci. USA 93, 11173-11178 (1996).
61. Chae, T. et al. Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 18, 29-42 (1997).
62. Sobue, K. et al. Interaction of neuronal Cdc2-like protein kinase with microtubule-associated protein tau. J. Biol. Chem. 275, 16673-16680 (2000).
63. Patrick, G. N. et al. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402, 615-622 (1999).
64. Ahlijanian, M. K. et al. Hyperphosphorylated tau and neurofilament and cytosketetal disruptions in mice overexpressing human p25, an activator of cdk5. Proc. Natl Acad. Sci. USA 97, 2910-2915 (2000).
65. Trommsdorff, M. et al. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97, 689-701 (1999).
66. Ware, M. L. et al. Aberrant splicing of a mouse disabled homolog, mdab1, in the scrambler mouse. Neuron 19, 239-249 (1997).
67. Fox, J. W. et al. Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron 21, 1315-1325 (1998).
68. Dulabon, L. et al. Reelin binds α3β1 integrin and inhibits neuronal migration. Neuron 27, 33-44 (2000).
69. D'Arcangelo, G. et al. A protein related to extracellular matrix proteins deleted in the mouse mutant reefer. Nature 374, 719-723 (1995).
70. 3H]thymidine autoradiography. Brain Res. 256, 293-302 (1982).
71. Pinto-Lord, M. C., Evrard, P. & Caviness, V. S. Jr Obstructed neuronal EM analysis. Brain Res. 256, 379-393 (1982).
72. Hong, S. E. et al. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nature Genet. 26, 93-96 (2000).
73. Howell, B. W., Gerter, F. B. & Cooper, J. A. Mouse disabled (mDab1): a Src binding protein implicated in neuronal development. EMBO J. 16, 121-132 (1997).
74. Sheldon, M. et al. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389, 730-733 (1997).
75. D'Arcangelo, G. et al. Reelin is a ligand for lipoprotein receptors. Neuron 24, 471-479 (1999).
76. Hiesberger, T. et al. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24, 481-489 (1999).
77. Nikolic, M., Chou, M. M., Lu, W., Mayer, B. J. & Tsai, L. H. The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 395, 194-193 (1998).