Neuronal polarity in CNS development

Genes and Development

Volumn 20, Issue 19, 2006, Pages 2639-2647

  Solecki, David J ^a   Govek, Eve Ellen ^a   Tomoda, Toshifumi ^a,b   Hatten, Mary E ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Axon outgrowth; CNS development; Migration; Neurogenesis; Polarity; Synaptogenesis

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; MESSENGER RNA; PROTEIN; PROTEIN PAR; UNCLASSIFIED DRUG;

CAENORHABDITIS ELEGANS; CELL POLARITY; CENTRAL NERVOUS SYSTEM FUNCTION; CENTROSOME; CEREBELLUM CORTEX; CYTOLOGY; DEVELOPMENTAL STAGE; DROSOPHILA; MOLECULAR GENETICS; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPTOGENESIS; ZYGOTE;

ANIMALS; CAENORHABDITIS ELEGANS PROTEINS; CELL POLARITY; CENTRAL NERVOUS SYSTEM; HUMANS; MODELS, BIOLOGICAL; NEURONS;

CAENORHABDITIS ELEGANS; MAMMALIA; VERTEBRATA;

EID: 33749338937     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1462506     Document Type: Review

References (88)

1. Anthony, T.E., Klein, C., Fishell, G., and Heintz, N. 2004. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41: 881-890.
2. Biederer, T. and Sudhof, T.C. 2001. CASK and protein 4.1 support F-actin nucleation on neurexins. J. Biol. Chem. 276: 47869-47876.
3. Biederer, T., Sara, Y., Mozhayeva, M., Atasoy, D., Liu, X., Kavalali, E.T., and Sudhof, T.C. 2002. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297: 1525-1531.
4. Castellani, V., Chedotal, A., Schachner, M., Faivre-Sarrailh, C., and Rougon, G. 2000. Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance. Neuron 27: 237-249.
5. Castellani, V., De Angelis, E., Kenwrick, S., and Rougon, G. 2002. Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO J. 21: 6348-6357.
6. Cau, J. and Hall, A. 2005. Cdc42 controls the polarity of the actin and microtubule cytoskeletons through two distinct signal transduction pathways. J. Cell Sci. 118: 2579-2587.
7. Chao, D.S., Hay, J.C., Winnick, S., Prekeris, R., Klumperman, J., and Scheller, R.H. 1999. SNARE membrane trafficking dynamics in vivo. J. Cell Biol. 144: 869-881.
8. Chen, X. and Macara, I.G. 2005. Par-3 controls tight junction assembly through the Rac exchange factor Tiam1. Nat. Cell Biol. 7: 262-269.
9. Darnell, J.C., Mostovetsky, O., and Darnell, R.B. 2005. FMRP RNA targets: Identification and validation. Genes Brain Behav. 4: 341-349.
10. Davis, L., Banker, G.A., and Steward, O. 1987. Selective dendritic transport of RNA in hippocampal neurons in culture. Nature 330: 477-479.
11. de Anda, F.C., Pollarolo, G., Da Silva, J.S., Camoletto, P.G., Feiguin, F., and Dotti, C.G. 2005. Centrosome localization determines neuronal polarity. Nature 436: 704-708.
12. Doe, C.Q. and Bowerman, B. 2001. Asymmetric cell division: Fly neuroblast meets worm zygote. Curr. Opin. Cell Biol. 13: 68-75.
13. Edmondson, J.C. and Hatten, M.E. 1987. Glial-guided granule neuron migration in vitro: A high-resolution time-lapse video microscopic study. J. Neurosci. 7: 1928-1934.
14. Etienne-Manneville, S. and Hall, A. 2001. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCζ. Cell 106: 489-498.
15. _. 2003. Cell polarity: Par6, aPKC and cytoskeletal crosstalk. Curr. Opin. Cell Biol. 15: 67-72.
16. Faulkner, N.E., Dujardin, D.L., Tai, C.Y., Vaughan, K.T., O'Connell, C.B., Wang, Y., and Vallee, R.B. 2000. A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat. Cell Biol. 2: 784-791.
17. Fuerstenberg, S., Broadus, J., and Doe, C.Q. 1998. Asymmetry and cell fate in the Drosophila embryonic CNS. Int. J. Dev. Biol. 42: 379-383.
18. Fukata, M., Nakagawa, M., Kuroda, S., and Kaibuchi, K. 2002. Effects of Rho family GTPases on cell-cell adhesion. Methods Mol. Biol. 189: 121-128.
19. Gao, L. and Macara, I.G. 2004. Isoforms of the polarity protein par6 have distinct functions. J. Biol. Chem. 279: 41557-41562.
20. Gleeson, J.G. 2001. Neuronal migration disorders. Ment. Retard. Dev. Disabil. Res. Rev. 7: 167-171.
21. Gleeson, J.G. and Walsh, C.A. 2000. Neuronal migration disorders: From genetic diseases to developmental mechanisms. Trends Neurosci. 23: 352-359.
22. Goetze, B., Tuebing, F., Xie, Y., Dorostkar, M.M., Thomas, S., Pehl, U., Boehm, S., Macchi, P., and Kiebler, M.A. 2006. The brain-specific double-stranded RNA-binding protein Staufen2 is required for dendritic spine morphogenesis. J. Cell Biol. 172: 221-231.
23. Goshima, Y., Nakamura, F., Strittmatter, P., and Strittmatter, S.M. 1995. Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 376: 509-514.
24. Goshima, G., Nedelec, F., and Vale, R.D. 2005. Mechanisms for focusing mitotic spindle poles by minus end-directed motor proteins. J. Cell Biol. 171: 229-240.
25. Gregory, W., Edmondson, J., Hatten, M., and Mason, C. 1988. Cytology and neuron-glial apposition of migrating cerebellar granule cells in vitro. J. Neurosci. 8: 1728-1738.
26. Grenningloh, G., Rehm, E.J., and Goodman, C.S. 1991. Genetic analysis of growth cone guidance in Drosophila: Fasciclin II functions as a neuronal recognition molecule. Cell 67: 45-57.
27. Hatten, M.E. 1999. Central nervous system neuronal migration. Annu. Rev. Neurosci. 22: 511-539.
28. _. 2002. New directions in neuronal migration. Science 297: 1660-1663.
29. _. 2005. LIS-less neurons don't even make it to the starting gate. J. Cell Biol. 170: 867-871.
30. Inagaki, N., Chihara, K., Arimura, N., Menager, C., Kawano, Y., Matsuo, N., Nishimura, T., Amano, M., and Kaibuchi, K. 2001. CRMP-2 induces axons in cultured hippocampal neurons. Nat. Neurosci. 4: 781-782.
31. Kelleher III, R.J., Govindarajan, A., Jung, H.Y., Kang, H., and Tonegawa, S. 2004a. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116: 467-479.
32. Kelleher III, R.J., Govindarajan, A., and Tonegawa, S. 2004b. Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44: 59-73.
33. Kenney, A.M. and Rowitch, D.H. 2000. Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol. Cell. Biol. 20: 9055-9067.
34. Kenney, A.M., Cole, M.D., and Rowitch, D.H. 2003. Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Development 130: 15-28.
35. Kenney, A.M., Widlund, H.R., and Rowitch, D.H. 2004. Hedge-hog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cerebellar neuronal precursors. Development 131: 217-228.
36. Kiebler, M.A., Hemraj, I., Verkade, P., Kohrmann, M., Fortes, P., Marion, R.M., Ortin, J., and Dotti, C.G. 1999. The mammalian staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: Implications for its involvement in mRNA transport. J. Neurosci. 19: 288-297.
37. Kim, S.K. 2000. Cell polarity: New PARtners for Cdc42 and Rac. Nat. Cell Biol. 2: E143-E145.
38. Kishi, M., Pan, Y.A., Crump, J.G., and Sanes, J.R. 2005. Mammalian SAD kinases are required for neuronal polarization. Science 307: 929-932.
39. Klezovitch, O., Fernandez, T.E., Tapscott, S.J., and Vasioukhin, V. 2004. Loss of cell polarity causes severe brain dysplasia in Lgl1 knockout mice. Genes & Dev. 18: 559-571.
40. Kohrmann, M., Luo, M., Kaether, C., DesGroseillers, L., Dotti, C.G., and Kiebler, M.A. 1999. Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol. Biol. Cell 10: 2945-2953.
41. Lai, T. and Garriga, G. 2004. The conserved kinase UNC-51 acts with VAB-8 and UNC-14 to regulate axon outgrowth in C. elegans. Development 131: 5991-6000.
42. Langevin, J., Le Borgne, R., Rosenfeld, F., Gho, M., Schweisguth, F., and Bellaiche, Y. 2005. Lethal giant larvae controls the localization of notch-signaling regulators numb, neuralized, and Sanpodo in Drosophila sensory-organ precursor cells. Curr. Biol. 1: 955-962.
43. Lefcort, F. and Bentley, D. 1989. Organization of cytoskeletal elements and organelles preceding growth cone emergence from an identified neuron in situ. J. Cell Biol. 108: 1737-1749.
44. Macara, I.G. 2004. Par proteins: Partners in polarization. Curr. Biol. 14: R160-R162.
45. Macchi, P., Hemraj, I., Goetze, B., Grunewald, B., Mallardo, M., and Kiebler, M.A. 2003. A GFP-based system to uncouple mRNA transport from translation in a single living neuron. Mol. Biol. Cell 14: 1570-1582.
46. Martin, K.C., Barad, M., and Kandel, E.R. 2000. Local protein synthesis and its role in synapse-specific plasticity. Curr. Opin. Neurobiol. 10: 587-592.
47. Nakada, C., Ritchie, K., Oba, Y., Nakamura, M., Hotta, Y., Iino, R., Kasai, R.S., Yamaguchi, K., Fujiwara, T., and Kusumi, A. 2003. Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat. Cell Biol. 5: 626-632.
48. Nishimura, T., Fukata, Y., Kato, K., Yamaguchi, T., Matsuura, Y., Kamiguchi, H., and Kaibuchi, K. 2003. CRMP-2 regulates polarized Numb-mediated endocytosis for axon growth. Nat. Cell Biol. 5: 819-826.
49. Nishimura, T., Yamaguchi, T., Kato, K., Yoshizawa, M., Nabeshima, Y., Ohno, S., Hoshino, M., and Kaibuchi, K. 2005. PAR-6-PAR-3 mediates Cdc42-induced Rac activation through the Rac GEFs STEF/Tiam1. Nat. Cell Biol. 7: 270-277.
50. Noctor, S.C., Martinez-Cerdeno, V., Ivic, L., and Kriegstein, A.R. 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7: 136-144.
51. O'Connell, C.B. and Wang, Y.L. 2000. Mammalian spindle orientation and position respond to changes in cell shape in a dynein-dependent fashion. Mol. Biol. Cell 11: 1765-1774.
52. Pellettieri, J. and Seydoux, G. 2002. Anterior-posterior polarity in C. elegans and Drosophila - PARallels and differences. Science 298: 2981946-2981950.
53. Petersen, P.H., Zou, K., Hwang, J.K., Jan, Y.N., and Zhong, W. 2002. Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature 419: 929-934.
54. Petersen, P.H., Zou, K., Krauss, S., and Zhong, W. 2004. Continuing role for mouse Numb and Numbl in maintaining progenitor cells during cortical neurogenesis. Nat. Neurosci. 7: 803-811.
55. Powell, S.K., Rivas, R.J., Rodriguez-Boulan, E., and Hatten, M.E. 1997. Development of polarity in cerebellar granule neurons. J. Neurobiol. 32: 223-236.
56. Rakic, P. 1971. Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus Rhesus. J. Comp. Neurol. 141: 283-312.
57. _. 1972. Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145: 61-83.
58. _. 1990. Principles of neural cell migration. Experientia 46: 882-891.
59. _. 2000. Molecular and cellular mechanisms of neuronal migration: Relevance to cortical epilepsies. Adv. Neurol. 84: 1-14.
60. Roegiers, F. and Jan, Y.N. 2000. Staufen: A common component of mRNA transport in oocytes and neurons? Trends Cell Biol. 10: 220-224.
61. Ross, M.E. and Walsh, C.A. 2001. Human brain malformations and their lessons for neuronal migration. Annu. Rev. Neurosci. 24: 1041-1070.
62. Sara, Y., Biederer, T., Atasoy, D., Chubykin, A., Mozhayeva, M.G., Sudhof, T.C., and Kavalali, E.T. 2005. Selective capability of SynCAM and neuroligin for functional synapse assembly. J. Neurosci. 25: 260-270.
63. Sauer, M.E. and Chittenden, A.C. 1959. Deoxyribonucleic acid content of cell nuclei in the neural tube of the chick embryo: Evidence for intermitotic migration of nuclei. Exp. Cell Res. 16: 1-6.
64. Schieffle, P., Fan, J., Choih, J., Fetter, R., and Serafine, T. 2000. Neruoligin expressed in nonneuronal cells triggers presynaptic development in contacting acons. Cell 101: 657-669.
65. Schwamborn, J.C. and Puschel, A.W. 2004. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat. Neurosci. 7: 923-929.
66. Shen, K. and Bargmann, C.I. 2003. The immunoglobulin superfamily protein SYG-1 determines the location of specific synapses in C. elegans. Cell 112: 619-630.
67. Shen, C.P., Knoblich, J.A., Chan, Y.M., Jiang, M.M., Jan, L.Y., and Jan, Y.N. 1998. Miranda as a multidomain adapter linking apically localized Inscuteable and basally localized Staufen and Prospero during asymmetric cell division in Drosophila. Genes & Dev. 12: 1837-1846.
68. Shen, K., Fetter, R.D., and Bargmann, C.I. 2004. Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1. Cell 116: 869-881.
69. Siller, K.H., Serr, M., Steward, R., Hays, T.S., and Doe, C.Q. 2005. Live imaging of Drosophila brain neuroblasts reveals a role for Lis1/dynactin in spindle assembly and mitotic checkpoint control. Mol. Biol. Cell 16: 5127-5140.
70. Solecki, D.J., Liu, X.L., Tomoda, T., Fang, Y., and Hatten, M.E. 2001. Activated Notch2 signaling inhibits differentiation of cerebellar granule neuron precursors by maintaining proliferation. Neuron 31: 557-568.
71. Solecki, D.J., Model, L., Gaetz, J., Kapoor, T.M., and Hatten, M.E. 2004. Par6α signaling controls glial-guided neuronal migration. Nat. Neurosci. 7: 1195-1203.
72. Spiegelman, B.M., Lopata, M.A., and Kirschner, M.W. 1979. Aggregation of microtubule initiation sites preceding neurite outgrowth in mouse neuroblastoma cells. Cell 16: 253-263.
73. Steegmaier, M., Yang, B., Yoo, J.S., Huang, B., Shen, M., Yu, S., Luo, Y., and Scheller, R.H. 1998. Three novel proteins of the syntaxin/SNAP-25 family. J. Biol. Chem. 273: 34171-34179.
74. Steward, O. and Schuman, E.M. 2001. Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 24: 299-325.
75. Steward, O. and Wallace, C.S. 1995. mRNA distribution within dendrites: Relationship to afferent innervation. J. Neurobiol. 26: 447-449.
76. Sun, T.Q., Lu, B., Feng, J.J., Reinhard, C., Jan, Y.N., Fantl, W.J., and Williams, L.T. 2001. PAR-1 is a Dishevelled-associated kinase and a positive regulator of Wnt signalling. Nat. Cell Biol. 3: 628-636.
77. Sun, Y., Goderie, S.K., and Temple, S. 2005. Asymmetric distribution of EGFR receptor during mitosis generates diverse CNS progenitor cells. Neuron 45: 873-886.
78. Tang, S.J., Meulemans, D., Vazquez, L., Colaco, N., and Schuman, E. 2001. A role for a rat homolog of staufen in the transport of RNA to neuronal dendrites. Neuron 32: 463-475.
79. Torban, E., Kor, C., and Gros, P. 2004. Van Gogh-like2 (Strabismus) and its role in planar cell polarity and convergent extension in vertebrates. Trends Genet. 20: 570-577.
80. Tsai, J.W., Chen, Y., Kriegstein, A.R., and Vallee, R.B. 2005. LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J. Cell Biol. 170: 935-945.
81. Wechsler-Reya, R.J. and Scott, M.P. 1999. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedge-hog. Neuron 22: 103-114.
82. Wiggin, G.R., Fawcett, J.P., and Pawson, T. 2005. Polarity proteins in axon specification and synaptogenesis. Dev. Cell 8: 803-816.
83. Wodarz, A., Ramrath, A., Grimm, A., and Knust, E. 2000. Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J. Cell Biol. 150: 1361-1374.
84. Young, A., Dictenberg, J.B., Purohit, A., Tuft, R., and Doxsey, S.J. 2000. Cytoplasmic dynein-mediated assembly of pericentrin and γ tubulin onto centrosomes. Mol. Biol. Cell 11: 2047-2056.
85. Yu, F., Kuo, C.T., and Jan, Y.N. 2006. Drosophila neuroblast asymmetric cell division: Recent advances and implications for stem cell biology. Neuron 51: 13-20.
86. Zarnescu, D.C., Jin, P., Betschinger, J., Nakamoto, M., Wang, Y., Dockendorff, T.C., Feng, Y., Jongens, T.A., Sisson, J.C., Knoblich, J.A., et al. 2005. Fragile X protein functions with lgl and the par complex in flies and mice. Dev. Cell 8: 43-52.
87. Zmuda, J.F. and Rivas, R. 1998. The Golgi apparatus and the centrosome are localized to the sites of newly emerging axons in cerebellar neurons in vitro. Cell Motil. Cytoskeleton 41: 18-38.
88. _. 2000. Actin disruption alters the localization of tau in the growth cones of cerebellar granule neurons. J. Cell Sci. 113: 2797-2809.