A crucial role for polysialic acid in developmental interneuron migration and the establishment of interneuron densities in the mouse prefrontal cortex

Development (Cambridge)

Volumn 141, Issue 15, 2014, Pages 3022-3032

  Kröcher, Tim ^a,b,d   Röckle, Iris ^a   Diederichs, Ute ^a   Weinhold, Birgit ^a   Burkhardt, Hannelore ^a   Yanagawa, Yuchio ^c   Gerardy Schahn, Rita ^a,b   Hildebrandt, Herbert ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

^c GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cortical interneuron migration; Mouse prefrontal cortex; NCAM; Neural cell adhesion molecule; Parvalbumin; Protein glycosylation; Somatostatin

Indexed keywords

CALBINDIN; CALRETININ; GLUTAMATE DECARBOXYLASE 67; GREEN FLUORESCENT PROTEIN; PARVALBUMIN; POLYSIALIC ACID; SOMATOSTATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL DENSITY; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; GANGLION; INTERNEURON; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; SLICE CULTURE;

CORTICAL INTERNEURON MIGRATION; MOUSE PREFRONTAL CORTEX; NCAM; NEURAL CELL ADHESION MOLECULE; PARVALBUMIN; PROTEIN GLYCOSYLATION; SOMATOSTATIN;

ANIMALS; APOPTOSIS; CALBINDINS; CELL MOVEMENT; GENETIC VARIATION; GREEN FLUORESCENT PROTEINS; INTERNEURONS; MICE; MICE, INBRED C57BL; NEURAL CELL ADHESION MOLECULES; NEURONS; PARVALBUMINS; PHENOTYPE; PREFRONTAL CORTEX; SIALIC ACIDS; SIALYLTRANSFERASES; SOMATOSTATIN;

EID: 84904662680     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.111773     Document Type: Article

References (85)

1. Alcantara, S, De Lecea, L., Del Rio, J. A., Ferrer, I. and Soriano, E. (1996). Transient colocalization of parvalbumin and calbindin D28k in the postnatal cerebral cortex: evidence for a phenotypic shift in developing nonpyramidal neurons. Eur. J. Neurosci. 8, 1329-1339.
2. Anastasiades, P. G. and Butt, S. J. B. (2011). Decoding the transcriptional basis for GABAergic interneuron diversity in the mouse neocortex. Eur. J. Neurosci. 34, 1542-1552.
3. Anderson, S. A., Eisenstat, D. D., Shi, L. and Rubenstein, J. L. R. (1997). Interneuron migration from basal forebrain to neocortex: dependence on DLX genes. Science 278, 474-476.
4. Anderson, S. A., Marin, O., Horn, C., Jennings, K. and Rubenstein, J. L. (2001). Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128, 353-363.
5. Angata, K., Long, J. M., Bukalo, O., Lee, W., Dityatev, A., Wynshaw-Boris, A., Schachner, M., Fukuda, M. and Marth, J. D. (2004). Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. J. Biol. Chem. 279, 32603-32613.
6. Angata, K., Huckaby, V., Ranscht, B., Terskikh, A., Marth, J. D. and Fukuda, M. (2007). Polysialic acid-directed migration and differentiation of neural precursors are essential for mouse brain development. Mol. Cell. Biol. 27, 6659-6668.
7. Anney, R., Klei, L., Pinto, D., Regan, R., Conroy, J., Magalhaes, T. R., Correia, C., Abrahams, B. S., Sykes, N., Pagnamenta, A. T. et al. (2010). A genome-wide scan for common alleles affecting risk for autism. Hum. Mol. Genet. 19, 4072-4082.
8. Arai, M., Yamada, K., Toyota, T., Obata, N., Haga, S., Yoshida, Y., Nakamura, K., Minabe, Y., Ujike, H., Sora, I. et al. (2006). Association between polymorphisms in the promoter region of the sialyltransferase 8B (SIAT8B) gene and schizophrenia. Biol. Psychiatry 59, 652-659.
9. Bellion, A., Baudoin, J.-P., Alvarez, C., Bornens, M. and Métin, C. (2005). Nucleokinesis in tangentially migrating neurons comprises two alternating phases: forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear. J. Neurosci. 25, 5691-5699.
10. Birjandian, Z., Narla, C. and Poulter, M. O. (2013). Gain control of gamma frequency activation by a novel feed forward disinhibitory loop: implications for normal and epileptic neural activity. Front. Neural Circuits7, 183.
11. Brennaman, L. H. and Maness, P. F. (2008). Developmental regulation of GABAergic interneuron branching and synaptic development in the prefrontal cortex by soluble neural cell adhesion molecule. Mol. Cell. Neurosci. 37, 781-793.
12. Brennaman, L. H. and Maness, P. F. (2010). NCAM in neuropsychiatric and neurodegenerative disorders. Adv. Exp. Med. Biol. 663, 299-317.
13. Brennaman, L. H., Kochlamazashvili, G., Stoenica, L., Nonneman, R. J., Moy, S. S., Schachner, M., Dityatev, A. and Maness, P. F. (2011). Transgenic mice overexpressing the extracellular domain of NCAM are impaired in working memory and cortical plasticity. Neurobiol. Dis. 43, 372-378.
14. Britto, J. M., Obata, K., Yanagawa, Y. and Tan, S.-S. (2006). Migratory response of interneurons to different regions of the developing neocortex. Cereb. Cortex16 Suppl. 1, i57-i63.
15. Brown, K. N., Chen, S., Han, Z., Lu, C.-H., Tan, X., Zhang, X.-J., Ding, L., LopezCruz, A., Saur, D., Anderson, S. A. et al. (2011). Clonal production and organization of inhibitory interneurons in the neocortex. Science 334, 480-486.
16. Calandreau, L., Márquez, C., Bisaz, R., Fantin, M. and Sandi, C. (2010). Differential impact of polysialyltransferase ST8SiaII and ST8SiaIV knockout on social interaction and aggression. Genes Brain Behav. 9, 958-967.
17. Chazal, G., Durbec, P., Jankovski, A., Rougon, G. and Cremer, H. (2000). Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J. Neurosci. 20, 1446-1457.
18. Cobos, I., Calcagnotto, M. E., Vilaythong, A. J., Thwin, M. T., Noebels, J. L., Baraban, S. C. and Rubenstein, J. L. R. (2005). Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat.
19. Curreli, S., Arany, Z., Gerardy-Schahn, R., Mann, D. and Stamatos, N. M. (2007). Polysialylated neuropilin-2 is expressed on the surface of human dendritic cells and modulates dendritic cell-T lymphocyte interactions. J. Biol. Chem. 282, 30346-30356.
20. Di Cristo, G., Chattopadhyaya, B., Kuhlman, S. J., Fu, Y., Bélanger, M.-C., Wu, C. Z., Rutishauser, U., Maffei, L. andHuang, Z. J. (2007). Activitydependent PSA expression regulates inhibitory maturation and onset of critical period plasticity. Nat. Neurosci. 10, 1569-1577.
21. Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M., Gerardy-Schahn, R., Cremer, H. and Dityatev, A. (2000). Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J. Neurosci. 20, 5234-5244.
22. Fisahn, A., Neddens, J., Yan, L. and Buonanno, A. (2009). Neuregulin-1 modulates hippocampal gamma oscillations: implications for schizophrenia. Cereb. Cortex 19, 612-618.
23. Flames, N., Long, J. E., Garratt, A. N., Fischer, T. M., Gassmann, M., Birchmeier, C., Lai, C., Rubenstein, J. L. R. and Maŕι n, O. (2004). Short-and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44, 251-261.
24. Fogarty, M., Grist, M., Gelman, D., Marin, O., Pachnis, V. and Kessaris, N. (2007). Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 27, 10935-10946.
25. Fonseca, M., DélRi{dotless}́ o, J. A., Marti{dotless}́ nez, A., Gómez, S. and Soriano, E. (1995). Development of cairetinin immunoreactivity in the neocortex of the rat. J. Comp. Neurol. 361, 177-192.
26. Friocourt, G., Liu, J. S., Antypa, M., Rakic, S., Walsh, C. A. and Parnavelas, J. G. (2007). Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J. Neurosci. 27, 3875-3883.
27. Frosch, M., Gorgen, I., Boulnois, G. J., Timmis, K. N. and Bitter-Suermann, D. (1985). NZB mouse system for production of monoclonal antibodies to weak bacterial antigens: isolation of an IgG antibody to the polysaccharide capsules of Escherichia coli K1 and group B meningococci. Proc. Natl. Acad. Sci. USA 82, 1194-1198.
28. Gabbott, P. L. A., Dickie, B. G. M., Vaid, R. R., Headlam, A. J. N. and Bacon, S. J. (1997). Local-circuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: morphology and quantitative distribution. J. Comp. Neurol. 377, 465-499.
29. Galuska, S. P., Oltmann-Norden, I., Geyer, H., Weinhold, B., Kuchelmeister, K., Hildebrandt, H., Gerardy-Schahn, R., Geyer, R. and Mühlenhoff, M. (2006). Polysialic acid profiles of mice expressing variant allelic combinations of the polysialyltransferases ST8SiaII and ST8SiaIV. J. Biol. Chem. 281, 31605-31615.
30. Galuska, S. P., Rollenhagen, M., Kaup, M., Eggers, K., Oltmann-Norden, I., Schiff, M., Hartmann, M., Weinhold, B., Hildebrandt, H., Geyer, R. et al. (2010). Synaptic cell adhesion molecule SynCAM 1 is a target for polysialylation in postnatal mouse brain. Proc. Natl. Acad. Sci. USA 107, 10250-10255.
31. Gelman, D. M. and Maŕι n, O. (2010). Generation of interneuron diversity in the mouse cerebral cortex. Eur. J. Neurosci. 31, 2136-2141.
32. Gilabert-Juan, J., Varea, E., Guirado, R., Blasco-Ibáñez, J. M., Crespo, C. and Nácher, J. (2012). Alterations in the expression of PSA-NCAM and synaptic proteins in the dorsolateral prefrontal cortex of psychiatric disorder patients. Neurosci. Lett. 530, 97-102.
33. Gonchar, Y. and Burkhalter, A. (1997). Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex 7, 347-358.
34. Härtig, W., Brauer, K. and Brückner, G. (1992). Wisteria floribunda agglutininlabelled nets surround parvalbumin-containing neurons. NeuroReport 3, 869-872.
35. Hikida, T., Jaaro-Peled, H., Seshadri, S., Oishi, K., Hookway, C., Kong, S., Wu, D., Xue, R., Andrade, M., Tankou, S. et al. (2007). Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans. Proc. Natl. Acad. Sci. USA 104, 14501-14506.
36. Hildebrandt, H., Becker, C., Mürau, M., Gerardy-Schahn, R. and Rahmann, H. (1998). Heterogeneous expression of the polysialyltransferases ST8Sia II and ST8Sia IV during postnatal rat brain development. J. Neurochem. 71, 2339-2348.
37. Hildebrandt, H., Mühlenhoff, M., Oltmann-Norden, I., Röckle, I., Burkhardt, H., Weinhold, B. and Gerardy-Schahn, R. (2009). Imbalance of neural cell adhesion molecule and polysialyltransferase alleles causes defective brain connectivity. Brain 132, 2831-2838.
38. Hildebrandt, H., Mühlenhoff, M. and Gerardy-Schahn, R. (2010). Polysialylation of NCAM. Adv. Exp. Med. Biol. 663, 95-109.
39. Hirn, M., Ghandour, M. S., Deagostini-Bazin, H. and Goridis, C. (1983). Molecular heterogeneity and structural evolution during cerebellar ontogeny detected by monoclonal antibody of the mouse cell surface antigen BSP-2. Brain Res. 265, 87-100.
40. Jakobsson, E., Schwarzer, D., Jokilammi, A. and Finne, J. (2012). Endosialidases: versatile tools for the study of polysialic acid. Top. Curr. Chem., doi: 10. 1007/128_2012_349.
41. Kaufman, M. H. (1992). The Atlas of Mouse Development. London: Academic Press.
42. Kawaguchi, Y. and Kubota, Y. (1997). GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex7, 476-
43. Kröcher, T., Malinovskaja, K., Jürgenson, M., Aonurm-Helm, A., Zharkovskaya, T., Kalda, A., Röckle, I., Schiff, M., Weinhold, B., Gerardy-Schahn, R. et al. (2013). Schizophrenia-like phenotype of polysialyltransferase ST8SIA2-deficient mice. Brain Struct. Funct., doi: 10. 1007/s00429-013-0638-z.
44. Lavdas, A. A., Grigoriou, M., Pachnis, V. and Parnavelas, J. G. (1999). The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 19, 7881-7888.
45. Lewis, D. A., Curley, A. A., Glausier, J. R. and Volk, D. W. (2012). Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia. Trends Neurosci. 35, 57-67.
46. Liodis, P., Denaxa, M., Grigoriou, M., Akufo-Addo, C., Yanagawa, Y. and Pachnis, V. (2007). Lhx6 activity is required for the normal migration and specification of cortical interneuron subtypes. J. Neurosci. 27, 3078-3089.
47. Luccardini, C., Hennekinne, L., Viou, L., Yanagida, M., Murakami, F., Kessaris, N., Ma, X., Adelstein, R. S., Mege, R.-M. and Metin, C. (2013). N-cadherin sustains motility and polarity of future cortical interneurons during tangential migration. J. Neurosci. 33, 18149-18160.
48. Marin, O. (2012). Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13, 107-120.
49. Marin, O., Valiente, M., Ge, X. and Tsai, L.-H. (2010). Guiding neuronal cell migrations. Cold Spring Harb. Perspect. Biol. 2, a001834.
50. Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G. and Wu, C. (2004). Interneurons of the neocortical inhibitorysystem. Nat. Rev. Neurosci. 5, 793-807.
51. McAuley, E. Z., Scimone, A., Tiwari, Y., Agahi, G., Mowry, B. J., Holliday, E. G., Donald, J. A., Weickert, C. S., Mitchell, P. B., Schofield, P. R. et al. (2012). Identification of sialyltransferase 8B as a generalized susceptibility gene for psychotic and mood disorders on chromosome 15q25-26. PLoS ONE7, e38172.
52. Mione, M. C., Danevic, C., Boardman, P., Harris, B. and Parnavelas, J. G. (1994). Lineage analysis reveals neurotransmitter (GABA or glutamate) but not calciumbinding protein homogeneity in clonally related cortical neurons. J. Neurosci. 14, 107-123.
53. Mühlenhoff, M., Rollenhagen, M., Werneburg, S., Gerardy-Schahn, R. and Hildebrandt, H. (2013). Polysialic acid: Versatile modification of NCAM, SynCAM 1 and neuropilin-2. Neurochem. Res. 38, 1134-1143.
54. Nacher, J., Guirado, R., Varea, E., Alonso-Llosa, G., Röckle, I. and Hildebrandt, H. (2010). Divergent impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid expression in immature neurons and interneurons ofthe adult cerebral cortex. Neuroscience 167, 825-837.
55. Nasrallah, I. M., McManus, M. F., Pancoast, M. M., Wynshaw-Boris, A. and Golden, J. A. (2006). Analysis of non-radial interneuron migration dynamics and its disruption in Lis1+/-mice. J. Comp. Neurol. 496, 847-858.
56. Ojima, H. (1993). Dendritic arborization patterns of cortical interneurons labeled with the lectin, Vicia villosa, and injected intracellularly with Lucifer yellow in aldehydefixed rat slices. J. Chem. Neuroanat. 6, 311-321.
57. Oltmann-Norden, I., Galuska, S. P., Hildebrandt, H., Geyer, R., GerardySchahn, R., Geyer, H. and Mühlenhoff, M. (2008). Impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid synthesis during postnatal mouse brain development. J. Biol. Chem. 283, 1463-1471.
58. Ong, E., Nakayama, J., Angata, K., Reyes, L., Katsuyama, T., Arai, Y. and Fukuda, M. (1998). Developmental regulation of polysialic acid synthesis in mouse directed by two polysialyltransferases, PST and STX. Glycobiology 8, 415-424.
59. Ono, K., Tomasiewicz, H., Magnuson, T. and Rutishauser, U. (1994). N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron 13, 595-609.
60. Paxinos, G. and Franklin, K. B. J. (2001). The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press.
61. Pillai-Nair, N., Panicker, A. K., Rodriguiz, R. M., Gilmore, K. L., Demyanenko, G. P., Huang, J. Z., Wetsel, W. C. and Maness, P. F. (2005). Neural cell adhesion molecule-secreting transgenic mice display abnormalities in GABAergic interneurons and alterations in behavior. J. Neurosci. 25, 4659-4671.
62. Polleux, F., Whitford, K. L., Dijkhuizen, P. A., Vitalis, T. and Ghosh, A. (2002). Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development 129, 3147-3160.
63. Potschka, H., Pekcec, A., Weinhold, B. and Gerardy-Schahn, R. (2008). Deficiency of neural cell adhesion molecule or its polysialylation modulates pharmacological effects of the AMPA receptor antagonist NBQX. Neuroscience 152, 1093-1098.
64. Powell, E. M., Mars, W. M. and Levitt, P. (2001). Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron 30, 79-89.
65. Powell, E. M., Campbell, D. B., Stanwood, G. D., Davis, C., Noebels, J. L. and Levitt, P. (2003). Genetic disruption of cortical interneuron development causes region-and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. J. Neurosci. 23, 622-631.
66. Powell, S. B., Sejnowski, T. J. and Behrens, M. M. (2012). Behavioral and neurochemical consequences of cortical oxidative stress on parvalbumininterneuron maturation in rodent models of schizophrenia. Neuropharmacology 62, 1322-1331.
67. Rhodes, K. E. and Fawcett, J. W. (2004). Chondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS?J. Anat. 204, 33-48.
68. Ross, C. A., Margolis, R. L., Reading, S. A., Pletnikov, M. and Coyle, J. T. (2006). Neurobiology of schizophrenia. Neuron 52, 139-153.
69. Rutishauser, U. (2008). Polysialic acid in the plasticity of the developing and adult vertebrate nervoussystem. Nat. Rev. Neurosci. 9, 26-35.
70. Schiff, M., Weinhold, B., Grothe, C. and Hildebrandt, H. (2009). NCAM and polysialyltransferase profiles match dopaminergic marker gene expression but polysialic acid is dispensable for development of the midbrain dopamine system. J. Neurochem. 110, 1661-1673.
71. Schiff, M., Röckle, I., Burkhardt, H., Weinhold, B. and Hildebrandt, H. (2011). Thalamocortical pathfinding defects precede degeneration of the reticular thalamic nucleus in polysialic acid-deficient mice. J. Neurosci. 31, 1302-1312.
72. Schnaar, R. L., Gerardy-Schahn, R. and Hildebrandt, H. (2014). Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol. Rev. 94, 461-518.
73. Schneider, C. A., Rasband, W. S. and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675.
74. Shen, S., Lang, B., Nakamoto, C., Zhang, F., Pu, J., Kuan, S.-L., Chatzi, C., He, S., Mackie, I., Brandon, N. J. et al. (2008). Schizophrenia-related neural and behavioral phenotypes in transgenic mice expressing truncated Disc1. J. Neurosci. 28, 10893-10904.
75. Steinecke, A., Gampe, C., Valkova, C., Kaether, C. and Bolz, J. (2012). Disrupted-in-Schizophrenia 1 (DISC1) is necessary for the correct migration of cortical interneurons. J. Neurosci. 32, 738-745.
76. Stummeyer, K., Dickmanns, A., Mühlenhoff, M., Gerardy-Schahn, R. and Ficner, R. (2005). Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage K1F. Nat. Struct. Mol. Biol. 12, 90-96.
77. Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J.-I., Obata, K. and Kaneko, T. (2003). Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J. Comp. Neurol. 467, 60-79.
78. Tanaka, D. H., Maekawa, K., Yanagawa, Y., Obata, K. and Murakami, F. (2006). Multidirectional and multizonal tangential migration of GABAergic interneurons in the developing cerebral cortex. Development 133, 2167-2176.
79. Tao, R., Li, C., Zheng, Y., Qin, W., Zhang, J., Li, X., Xu, Y., Shi, Y. Y., Feng, G. and He, L. (2007). Positive association between SIAT8B and schizophrenia in the Chinese Han population. Schizophr. Res. 90, 108-114.
80. Vaithianathan, T., Matthias, K., Bahr, B., Schachner, M., Suppiramaniam, V., Dityatev, A. and Steinhauser, C. (2004). Neural cell adhesion moleculeassociated polysialic acid potentiates alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor currents. J. Biol. Chem. 279, 47975-47984.
81. Valcanis, H. and Tan, S. S. (2003). Layer specification of transplanted interneurons in developing mouse neocortex. J. Neurosci. 23, 5113-5122.
82. Wang, Y., Li, G., Stanco, A., Long, J. E., Crawford, D., Potter, G. B., Pleasure, S. J., Behrens, T. and Rubenstein, J. L. R. (2011). CXCR4 and CXCR7 have distinct functions in regulating interneuron migration. Neuron69,61-76.
83. Wegner, F., Härtig, W., Bringmann, A., Grosche, J., Wohlfarth, K., Zuschratter, W. and Brückner, G. (2003). Diffuse perineuronal nets and modified pyramidal cells immunoreactive for glutamate and the GABA(A) receptor alpha1 subunit form a unique entity in rat cerebral cortex. Exp. Neurol. 184, 705-714.
84. Weinhold, B., Seidenfaden, R., Röckle, I., Mühlenhoff, M., Schertzinger, F., Conzelmann, S., Marth, J. D., Gerardy-Schahn, R. and Hildebrandt, H. (2005). Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J. Biol. Chem. 280, 42971-42977.
85. Xu, Q., Cobos, I., De La, C. E., Rubenstein, J. L. and Anderson, S. A. (2004). Origins of cortical interneuron subtypes. J. Neurosci. 24, 2612-2622.