Essential roles of leucine-rich glioma inactivated 1 in the development of embryonic and postnatal cerebellum

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Xie, Ya Jun ^a   Zhou, Liang ^a   Jiang, Nanwei ^b   Zhang, Nan ^c   Zou, Na ^a   Zhou, Lin ^a   Wang, Yin ^c   Cowell, John K ^d   Shen, Ying ^a  

^a Key Laboratory of Gastroenterology of Zhejiang Province   (China)

^b NINGBO UNIVERSITY   (China)

^c NINGXIA MEDICAL UNIVERSITY   (China)

^d MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LGI1 PROTEIN, MOUSE; NESTIN; NOTCH RECEPTOR; PROTEIN; SONIC HEDGEHOG PROTEIN;

ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CEREBELLUM; CYTOLOGY; DOWN REGULATION; GENETICS; KNOCKOUT MOUSE; MACROGLIA; MAMMALIAN EMBRYO; METABOLISM; MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBELLUM; DOWN-REGULATION; EMBRYO, MAMMALIAN; EPENDYMOGLIAL CELLS; HEDGEHOG PROTEINS; MICE; MICE, KNOCKOUT; NESTIN; PROTEINS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84929350648     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep07827     Document Type: Article

References (60)

1. Kalachikov, S. et al.Mutations in LGI1 cause autosomal-dominant partial epilepsy with auditory features. Nat. Genet. 30, 335-341 (2002).
2. Gu,W., Brodtkorb, E., Steinlein, O. K. LGI1 is mutated in familial temporal lobe epilepsy characterized by aphasic seizures. Ann. Neurol. 52, 364-367 (2002).
3. Senechal, K. R., Thaller, C., Noebels, J. L. ADPEAF mutations reduce levels of secreted LGI1, a putative tumor suppressor protein linked to epilepsy. Hum. Mol. Genet. 14, 1613-1620 (2005).
4. Kegel, L., Aunin, E., Meijer, D., Bermingham, J. R. LGI proteins in the nervous system. ASN Neuro. 5, 167-181 (2013).
5. Fukata, Y. et al. Epilepsy-related ligand/receptor complex LGI1 and ADAM22 regulate synaptic transmission. Science 313, 1792-1795 (2006).
6. Chabrol, E. et al. Electroclinical characterization of epileptic seizures in leucinerich, glioma-inactivated 1-deficient mice. Brain 133, 2749-2762 (2010).
7. Fukata, Y. et al. Disruption of LGI1-linked synaptic complex causes abnormal synaptic transmission and epilepsy. Proc. Natl. Acad. Sci. USA 107, 3799-3804 (2010).
8. Yu, Y. E. et al. Lgi1 null mutantmice exhibit myoclonic seizures and CA1 neuronal hyperexcitability. Hum. Mol. Genet. 19, 1702-1711 (2010).
9. Schulte, U. et al. The epilepsy-linked Lgi1 protein assembles into presynaptic Kv1 channels and inhibits inactivation by Kvbeta1. Neuron 49, 697-706 (2006).
10. Zhou, Y. D. et al. Arrested maturation of excitatory synapses in autosomal dominant lateral temporal lobe epilepsy. Nat. Med. 15, 1208-1214 (2009).
11. Sagane, K., Ishihama, Y., Sugimoto, H. LGI1 and LGI4 bind to ADAM22, ADAM23 and ADAM11. Inter. J. Biol. Sci. 4, 387-396 (2008).
12. Thomas, R. et al. LGI1 is a Nogo receptor 1 ligand that antagonizes myelin-based growth inhibition. J. Neurosci. 30, 6607-6612 (2010).
13. Head, K. et al.Defining the expression pattern of the LGI1 gene in BAC transgenic mice. Mamm. Genome 18, 328-337 (2007).
14. Silva, J., Wang, G., Cowell, J. K. The temporal and spatial expression pattern of the LGI1 epilepsy predisposition gene during mouse embryonic cranial development. BMC Neurosci. 12, 43 (2011).
15. Kusuzawa, S. et al. Leucine-rich glioma inactivated 1 (Lgi1), an epilepsy-related secreted protein, has a nuclear localization signal and localizes to both the cytoplasm and the nucleus of the caudal ganglionic eminence neurons. Eur. J. Neurosci. 36, 2284-2292 (2012).
16. Silva, J., Sharma, S., Hughes, B., Yu, Y. E.& Cowell, J. K. Homozygous inactivation of the Lgi1 gene results in hypomyelination in the peripheral and central nervous system. J. Neurosci. Res. 88, 3328-3336 (2010).
17. Mangiarini, L. et al. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87, 493-506 (1996).
18. Miale, I. L., Sidman, R. L. An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp. Neurol. 4, 277-296 (1961).
19. Wang, V. Y., Zoghbi, H. Y. Genetic regulation of cerebellar development. Nat. Rev. Neurosci. 2, 484-491 (2001).
20. Sudarov, A., Joyner, A. L. Cerebellum morphogenesis: the foliation pattern is orchestrated by multi-cellular anchoring centers. Neural. Dev. 2, 26 (2007).
21. Miner, J. H., Li, C., Mudd, J. L., Go, G., Sutherland, A. E. Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation. Development 131, 2247-2256 (2004).
22. Yurchenco, P. D., Patton, B. L. Developmental and pathogenic mechanisms of basement membrane assembly. Curr. Pharm. Des. 15, 1277-1294 (2009).
23. Lendahl,U., Zimmerman, L. B., McKay, R. D. CNS stem cells express a new class of intermediate filament protein. Cell 60, 585-595 (1990).
24. Inoue, T., Nakamura, S., Osumi, N. Fate mapping of the mouse prosencephalic neural plate. Dev. Biol. 219, 373-383 (2000).
25. Engelkamp, D., Rashbass, P., Seawright, A., van Heyningen, V. Role of Pax6 in development of the cerebellar system. Development 126, 3585-3596 (1999).
26. Osumi, N., Shinohara, H., Numayama-Tsuruta, K., Maekawa, M. Concise review: Pax6 transcription factor contributes to both embryonic and adult neurogenesis as a multifunctional regulator. Stem Cells 26, 1663-1672 (2008).
27. Lin, J. C., Cepko, C. L. Granule cell raphes and parasagittal domains of Purkinje cells: complementary patterns in the developing chick cerebellum. J. Neurosci. 18, 9342-9353 (1998).
28. Dahmane, N., Ruiz i Altaba, A. Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126, 3089-3100 (1999).
29. Wallace, V. A. Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr. Biol. 9, 445-448 (1999).
30. Wechsler-Reya, R. J., Scott, M. P. Control of neuronal precursor proliferation in the cerebellum by Sonic hedgehog. Neuron 22, 103-114 (1999).
31. Xu, H. et al. Bergmann glia function in granule cell migration during cerebellum development. Mol. Neurobiol. 47, 833-844 (2013).
32. Feng, L., Hatten, M. E., Heintz, N. Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12, 895-908 (1994).
33. Soriano, E., Alvarado-Mallart, R. M., Dumesnil, N., Del Ró, J. A., Sotelo, C. Cajal-Retzius cells regulate the radial glia phenotype in the adult and developing cerebellum and alter granule cell migration. Neuron 18, 563-577 (1997).
34. Kuang, Y. et al. Dicer and MiR-9 are required for proper Notch1 signaling and the Bergmann glial phenotype in the developing mouse cerebellum. Glia 60, 1734-1746 (2012).
35. Brunne, B. et al. Origin, maturation & astroglial transformation of secondary radial glial cells in the developing dentate gyrus. Glia 58, 1553-1569 (2010).
36. Stipursky, J., Gomes, F. C. TGF-b1/SMAD signaling induces astrocyte fate commitment in vitro: implications for radial glia development. Glia 55, 1023-1033 (2007).
37. Stipursky, J., Francis, D., Gomes, F. C. Activation of MAPK/PI3K/SMAD pathways by TGF-b(1) controls differentiation of radial glia into astrocytes in vitro. Dev. Neurosci. 34, 68-81 (2012).
38. Schinstine, M., Lacovitti, L. Expression of neuronal antigens by astrocytes derived from EGF-generated neuroprogenitor cells. Exp. Neurol. 141, 67-78 (1996).
39. Shi, Y. et al. Expression and function of orphan nuclear receptor TLX in adult neural stem cells. Nature 427, 78-83 (2004).
40. Frederiksen, K., McKay, R. D. Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J. Neurosci. 8, 1144-1151 (1988).
41. Dahlstrand, J., Lardelli, M., Lendahl, U. Nestin mRNA expression correlates with the central nervous system progenitor cell state in many, but not all, regions of developing central nervous system. Brain Res. Dev. Brain Res. 84, 109-129 (1995).
42. Anthony, T. E., Mason, H. A., Gridley, T., Fishell, G., Heintz, N. Brain lipidbinding protein is a direct target of Notch signaling in radial glial cells. Genes Dev. 19, 1028-1033 (2005).
43. Gaiano, N., Nye, J. S., Fishell, G. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26, 395-404 (2000).
44. Patten, B. A., Peyrin, J. M., Weinmaster, G., Corfas, G. Sequential signaling through Notch1 and erbB receptors mediates radial glia differentiation. J. Neurosci. 23, 6132-6140 (2003).
45. Schmid, R. S. et al. Neuregulin 1-erbB2 signaling is required for the establishment of radial glia and their transformation into astrocytes in cerebral cortex. Proc. Natl. Acad. Sci. USA 100, 4251-4256 (2003).
46. Gaiano, N., Fishell, G. The role of notch in promoting glial and neural stem cell fates. Annu. Rev. Neurosci. 25, 471-490 (2002).
47. Kopan, R., Ilagan, M. X. G. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137, 216-233 (2009).
48. Hu, X., He, W., Luo, X., Tsubota, K. E., Yan, R. BACE1 regulates hippocampal astrogenesis via the Jagged1-Notch pathway. Cell Rep. 4, 40-49 (2013).
49. Park, W. J. et al. Leucine-rich glioma inactivated 3 associates with syntaxin 1. Neurosci. Lett. 444, 240-244 (2008).
50. Leonardi, E. et al. A computational model of the LGI1 protein suggests a common binding site for ADAM protein. PLoS One 6, e18142 (2011).
51. Reiss, K., Saftig, P. The "a disintegrin and metalloprotease" (ADAM) family of sheddases: physiological and cellular functions. Semin. Cell Dev. Biol. 20, 126-137 (2009).
52. Novak, U. ADAM proteins in the brain. J. Clin. Neurosci. 11, 227-235 (2004).
53. Kunapuli, P., Lo, K., Hawthorn, L., Cowell, J. K. Reexpression of LGI1 in glioma cells results in dysregulation of genes implicated in the canonical axon guidance pathway. Genomics 95, 93-100 (2010).
54. Bray, S. J. Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7, 678-689 (2006).
55. Wang, D. J. et al. Long-term potentiation at cerebellar parallel fiber-Purkinje cell synapses requires presynaptic and postsynaptic signaling cascades. J. Neurosci. 34, 2355-2364 (2014).
56. Li, H., Berlin, Y., Hart, R. P., Grumet, M. Microtubules are critical for radial glial morphology: possible regulation by MAPs and MARKs. Glia 44, 37-46 (2003).
57. Aoyama, K., Matsumura, N., Watanabe, M., Nakaki, T. Oxidative stress on EAAC1 is involved in MPTP-induced glutathione depletion and motor dysfunction. Eur. J. Neurosci. 27, 20-30 (2008).
58. Zhu, J. et al. Chronic zinc exposure decreases the surface expression of NR2Acontaining NMDA receptors in cultured hippocampal neurons. PLoS One 7, e46012 (2012).
59. Ji, Y. F. et al. Upregulation of glutamate transporter GLT-1 by mTOR-Akt-NF-kB cascade in astrocytic oxygen-glucose deprivation. Glia 61, 1959-1975 (2013).
60. Shao, C. Y. et al. Distinct functions of nuclear distribution proteins LIS1, Ndel1 and NudCL in regulating axonal mitochondrial transport. Traffic 14, 785-797 (2013).