The role of T-cadherin in axonal pathway formation in neocortical circuits

Development (Cambridge)

Volumn 141, Issue 24, 2014, Pages 4784-4793

  Hayano, Yuki ^a   Zhao, Hong ^a   Kobayashi, Hiroaki ^a   Takeuchi, Kosei ^b   Norioka, Shigemi ^a   Yamamoto, Nobuhiko ^a  

^a OSAKA UNIVERSITY   (Japan)

^b AICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

Adhesion; Cadherin; Fasciculation; Neocortex; Pathfinding

Indexed keywords

CADHERIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 6C9; T CADHERIN; UNCLASSIFIED DRUG; H-CADHERIN;

ANIMAL CELL; ARTICLE; BRAIN CELL; BRAIN CORTEX; BRAIN DEVELOPMENT; CONTROLLED STUDY; CORPUS CALLOSUM; INTERMEDIATE ZONE; NEOCORTEX; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; RAT; RNA INTERFERENCE; AMINO ACID SEQUENCE; ANIMAL; CYTOLOGY; ELECTROPORATION; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; MOLECULAR GENETICS; NERVE FIBER; NERVE TRACT; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; SEQUENCE ANALYSIS; WESTERN BLOTTING;

RATTUS;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, NEWBORN; AXONS; BLOTTING, WESTERN; CADHERINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ELECTROPORATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; NEOCORTEX; NEURAL PATHWAYS; RATS; RNA INTERFERENCE; SEQUENCE ANALYSIS, PROTEIN;

EID: 84919360167     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.108290     Document Type: Article

References (76)

1. Arlotta, P., Molyneaux, B. J., Chen, J., Inoue, J., Kominami, R. and Macklis, J. D. (2005). Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45, 207-221.
2. Bastiani, M. J., Harrelson, A. L., Snow, P. M. and Goodman, C. S. (1987). Expression of fasciclin I and II glycoproteins on subsets of axon pathways during neuronal development in the grasshopper. Cell 48, 745-755.
3. Bentley, D. and Caudy, M. (1983). Pioneer axons lose directed growth after selective killing of guidepost cells. Nature 304, 62-65.
4. Bentley, D. and Keshishian, H. (1982). Pathfinding by peripheral pioneer neurons in grasshoppers. Science 218, 1082-1088.
5. Bicknese, A. R., Sheppard, A. M., O’Leary, D. D. and Pearlman, A. L. (1994). Thalamocortical axons extend along a chondroitin sulfate proteoglycan-enriched pathway coincident with the neocortical subplate and distinct from the efferent path. J. Neurosci. 14, 3500-3510.
6. Buttiglione, M., Revest, J. M., Pavlou, O., Karagogeos, D., Furley, A., Rougon, G. and Faivre-Sarrailh, C. (1998). A functional interaction between the neuronal adhesion molecules TAG-1 and F3 modulates neurite outgrowth and fasciculation of cerebellar granule cells. J. Neurosci. 18, 6853-6870.
7. Catalano, S. M., Robertson, R. T. and Killackey, H. P. (1991). Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat. Proc. Natl. Acad. Sci. USA 88, 2999-3003.
8. Chedotal, A., Pourquie, O. and Sotelo, C. (1995). Initial tract formation in the brain of the chick embryo: selective expression of the BEN/SC1/DM-GRASP cell adhesion molecule. Eur. J. Neurosci. 7, 198-212.
9. Chen, B., Schaevitz, L. R. and McConnell, S. K. (2005). Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc. Natl. Acad. Sci. USA 102, 17184-17189.
10. Ciatto, C., Bahna, F., Zampieri, N., VanSteenhouse, H. C., Katsamba, P. S., Ahlsen, G., Harrison, O. J., Brasch, J., Jin, X., Posy, S. et al. (2010). T-cadherin structures reveal a novel adhesive binding mechanism. Nat. Struct. Mol. Biol. 17, 339-347.
11. Cloutier, J.-F., Sahay, A., Chang, E. C., Tessier-Lavigne, M., Dulac, C., Kolodkin, A. L. and Ginty, D. D. (2004). Differential requirements for semaphorin 3F and Slit-1 in axonal targeting, fasciculation, and segregation of olfactory sensory neuron projections. J. Neurosci. 24, 9087-9096
12. Cohen, N. R., Taylor, J. S. H., Scott, L. B., Guillery, R. W., Soriano, P. and Furley, A. J. W. (1998). Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr. Biol. 8, 26-33.
13. Denzel, M. S., Scimia, M.-C., Zumstein, P. M., Walsh, K., Ruiz-Lozano, P. and Ranscht, B. (2010). T-cadherin is critical for adiponectin-mediated cardioprotection in mice. J. Clin. Invest. 120, 4342-4352.
14. Dodd, J. and Jessell, T. M. (1988). Axon guidance and the patterning of neuronal projections in vertebrates. Science 242, 692-699
15. Fredette, B. J. and Ranscht, B. (1994). T-cadherin expression delineates specific regions of the developing motor axon-hindlimb projection pathway. J. Neurosci. 14, 7331-7346.
16. Fredette, B. J., Miller, J. and Ranscht, B. (1996). Inhibition of motor axon growth by T-cadherin substrata. Development 122, 3163-3171.
17. Fujimori, K. E., Takeuchi, K., Yazaki, T., Uyemura, K., Nojyo, Y. and Tamamki, N. (2000). Expression of L1 and TAG-1 in the corticospinal, callosal, and hippocampal commissural neurons in the developing rat telencephalon as revealed by retrograde and in situ hybridization double labeling. J. Comp. Neurol. 417, 275-288.
18. Fujita, S. C., Zipursky, S. L., Benzer, S., Ferrus, A. and Shotwell, S. L. (1982). Monoclonal antibodies against the Drosophila nervous system. Proc. Natl. Acad. Sci. USA 79, 7929-7933.
19. Fukuchi-Shimogori, T. and Grove, E. A. (2001). Neocortex patterning by the secreted signaling molecule FGF8. Science 294, 1071-1074.
20. Fukuda, T., Kawano, H., Ohyama, K., Li, H. P., Takeda, Y., Oohira, A. and Kawamura, K. (1997). Immunohistochemical localization of neurocan and L1 in the formation of thalamocortical pathway of developing rats. J. Comp. Neurol. 382, 141-152.
21. Han, W., Kwan, K. Y., Shim, S., Lam, M. M. S., Shin, Y., Xu, X., Zhu, Y., Li, M. and Sestan, N. (2011). TBR1 directly represses Fezf2 to control the laminar origin and development of the corticospinal tract. Proc. Natl. Acad. Sci. USA 108, 3041-3046.
22. Hatanaka, Y., Matsumoto, T., Yanagawa, Y., Fujisawa, H., Murakami, F. and Masu, M. (2009). Distinct roles of neuropilin 1 signaling for radial and tangential extension of callosal axons. J. Comp. Neurol. 514, 215-225.
23. Henke-Fahle, S., Mann, F., Gotz, M., Wild, K. and Bolz, J. (1996). Dual action of a carbohydrate epitope on afferent and efferent axons in cortical development. J. Neurosci. 16, 4195-4206.
24. Hevner, R. F., Shi, L., Justice, N., Hsueh, Y.-P., Sheng, M., Smiga, S., Bulfone, A., Goffinet, A. M., Campagnoni, A. T. and Rubenstein, J. L. R. (2001). Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29, 353-366
25. Hug, C., Wang, J., Ahmad, N. S., Bogan, J. S., Tsao, T.-S. and Lodish, H. F. (2004). T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc. Natl. Acad. Sci. USA 101, 10308-10313.
26. Imai, T., Yamazaki, T., Kobayakawa, R., Kobayakawa, K., Abe, T., Suzuki, M. and Sakano, H. (2009). Pre-target axon sorting establishes the neural map topography. Science 325, 585-590.
27. Inoue, T., Tanaka, T., Suzuki, S. C. and Takeichi, M. (1998). Cadherin-6 in the developing mouse brain: expression along restricted connection systems and synaptic localization suggest a potential role in neuronal circuitry. Dev. Dyn. 211, 338-351.
28. Jaworski, A. and Tessier-Lavigne, M. (2012). Autocrine/juxtaparacrine regulation of axon fasciculation by Slit-Robo signaling. Nat. Neurosci. 15, 367-369.
29. Kawasaki, T., Bekku, Y., Suto, F., Kitsukawa, T., Taniguchi, M., Nagatsu, I., Nagatsu, T., Itoh, K., Yagi, T. and Fujisawa, H. (2002). Requirement of neuropilin 1-mediated Sema3A signals in patterning of the sympathetic nervous system. Development 129, 671-680.
30. Lai, T., Jabaudon, D., Molyneaux, B. J., Azim, E., Arlotta, P., Menezes, J. R. L. and Macklis, J. D. (2008). SOX5 controls the sequential generation of distinct corticofugal neuron subtypes. Neuron 57, 232-247.
31. Lebrand, C., Cases, O., Adelbrecht, C., Doye, A., Alvarez, C., El Mestikawy, S., Seif, I. and Gaspar, P. (1996). Transient uptake and storage of serotonin in developing thalamic neurons. Neuron 17, 823-835.
32. Lickiss, T., Cheung, A. F. P., Hutchinson, C. E., Taylor, J. S. H. and Molnar, Z. (2012). Examining the relationship between early axon growth and transcription factor expression in the developing cerebral cortex. J. Anat. 220, 201-211
33. Maness, P. F. and Schachner, M. (2007). Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 10, 19-26.
34. Marthiens, V., Gavard, J., Padilla, F., Monnet, C., Castellani, V., Lambert, M. and Mege, R. M. (2005). A novel function for cadherin-11 in the regulation of motor axon elongation and fasciculation. Mol. Cell. Neurosci. 28, 715-726
35. Matsunaga, E., Nambu, S., Oka, M. and Iriki, A. (2013). Differential cadherin expression in the developing postnatal telencephalon of a New World monkey. J. Comp. Neurol. 521, 4027-4060.
36. McConnell, S. K., Ghosh, A. and Shatz, C. J. (1989). Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245, 978-982.
37. McGeorge, A. J. and Faull, R. L. M. (1989). The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29, 503-537.
38. McKenna, W. L., Betancourt, J., Larkin, K. A., Abrams, B., Guo, C., Rubenstein, J. L. R. and Chen, B. (2011). Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J. Neurosci. 31, 549-564
39. Molnar, Z., Adams, R. and Blakemore, C. (1998a). Mechanisms underlying theearly establishment of thalamocortical connections in the rat. J. Neurosci. 18, 5723-5745.
40. Molnar, Z., Adams, R., Goffinet, A. M. and Blakemore, C. (1998b). The role of the first postmitotic cortical cells in the development of thalamocortical innervation in the reeler mouse. J. Neurosci. 18, 5746-5765.
41. Molnar, Z., Garel, S., Lopez-Bendito, G., Maness, P. and Price, D. J. (2012). Mechanisms controlling the guidance of thalamocortical axons through the embryonic forebrain. Eur. J. Neurosci. 35, 1573-1585.
42. Molyneaux, B. J., Arlotta, P., Hirata, T., Hibi, M. and Macklis, J. D. (2005). Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 47, 817-831.
43. Molyneaux, B. J., Arlotta, P., Fame, R. M., MacDonald, J. L., MacQuarrie, K. L. and Macklis, J. D. (2009). Novel subtype-specific genes identify distinct subpopulations of callosal projection neurons. J. Neurosci. 29, 12343-12354
44. Nakagawa, Y., Johnson, J. E. and O’Leary, D. D. (1999). Graded and arealexpression patterns of regulatory genes and cadherins in embryonic neocortex independent of thalamocortical input. J. Neurosci. 19, 10877-10885.
45. Nakashiba, T., Nishimura, S., Ikeda, T. and Itohara, S. (2002). Complementary expression and neurite outgrowth activity of netrin-G subfamily members. Mech. Dev. 111, 47-60.
46. Niquille, M., Garel, S., Mann, F., Hornung, J.-P., Otsmane, B., Chevalley, S., Parras, C., Guillemot, F., Gaspar, P., Yanagawa, Y. et al. (2009). Transient neuronal populations are required to guide callosal axons: a role for semaphorin 3C. PLoS Biol. 7, pe1000230.
47. Noctor, S. C., Martınez-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.
48. Ohyama, K., Tan-Takeuchi, K., Kutsche, M., Schachner, M., Uyemura, K. and Kawamura, K. (2004). Neural cell adhesion molecule L1 is required for fasciculation and routing of thalamocortical fibres and corticothalamic fibres. Neurosci. Res. 48, 471-475.
49. Oohira, A., Matsui, F., Watanabe, E., Kushima, Y. and Maeda, N. (1994). Developmentally regulated expression of a brain specific species of chondroitin sulfate proteoglycan, neurocan, identified with a monoclonal antibody 1G2 in the rat cerebrum. Neuroscience 60, 145-157.
50. Paradis, S., Harrar, D. B., Lin, Y., Koon, A. C., Hauser, J. L., Griffith, E. C., Zhu, L., Brass, L. F., Chen, C. and Greenberg, M. E. (2007). An RNAi-based approach identifies molecules required for glutamatergic and GABAergic synapse development. Neuron 53, 217-232.
51. Patel, N. H., Snow, P. M. and Goodman, C. S. (1987). Characterization and cloning of fasciclin III: a glycoprotein expressed on a subset of neurons and axon pathways in Drosophila. Cell 48, 975-988.
52. Pike, S. H., Melancon, E. F. and Eisen, J. S. (1992). Pathfinding by zebrafish motoneurons in the absence of normal pioneer axons. Development 114, 825-831.
53. Piper, M., Plachez, C., Zalucki, O., Fothergill, T., Goudreau, G., Erzurumlu, R., Gu, C. and Richards, L. J. (2009). Neuropilin 1-Sema signaling regulates crossing of cingulate pioneering axons during development of the corpus callosum. Cereb. Corex 19 Suppl. 1, i11-i21.
54. Prandovszky, E., Horvath, S., Gellert, L., Kovacs, S. K., Janka, Z., Toldi, J., Shukla, D. and Valyi-Nagy, T. (2008). Nectin-1 (HveC) is expressed at high levels in neural subtypes that regulate radial migration of cortical and cerebellar neurons of the developing human and murine brain. J. Neurovirol. 14, 164-172.
55. Richards, L. J., Koester, S. E., Tuttle, R. and O’Leary, D. D. (1997). Directed growth of early cortical axons is influenced by a chemoattractant released from an intermediate target. J. Neurosci. 17, 2445-2458.
56. Rivero, O., Sich, S., Popp, S., Schmitt, A., Franke, B. and Lesch, K.-P. (2013). Impact of the ADHD-susceptibility gene CDH13 on development and function of brain networks. Eur. Neuropsychopharmacol. 23, 492-507.
57. Sacristan, M. P., Vestal, D. J., Dours-Zimmermann, M. T. and Ranscht, B. (1993). T-cadherin 2: molecular characterization, function in cell adhesion, and coexpression with T-cadherin and N-cadherin. J. Neurosci. Res. 34, 664-680
58. Saito, T. and Nakatsuji, N. (2001). Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev. Biol. 240, 237-246.
59. Sato, Y., Hirata, T., Ogawa, M. and Fujisawa, H. (1998). Requirement for early- generated neurons recognized by monoclonal antibody lot1 in the formation of lateral olfactory tract. J. Neurosci. 18, 7800-7810.
60. Satoda, M., Takagi, S., Ohta, K., Hirata, T. and Fujisawa, H. (1995). Differential expression of two cell surface proteins, neuropilin and plexin, in Xenopus olfactory axon subclasses. J. Neurosci. 15, 942-955.
61. Schmitz, C., Wacker, I. and Hutter, H. (2008). The Fat-like cadherin CDH-4 controls axon fasciculation, cell migration and hypodermis and pharynx development in Caenorhabditis elegans. Dev. Biol. 316, 249-259
62. Schwartz, M. L., Rakic, P. and Goldman-Rakic, P. S. (1991). Early phenotype expression of cortical neurons: evidence that a subclass of migrating neurons have callosal axons. Proc. Natl. Acad. Sci. USA 88, 1354-1358.
63. Suzuki, S. C., Inoue, T., Kimura, Y., Tanaka, T. and Takeichi, M. (1997). Neuronal circuits are subdivided by differential expression of type-II classic cadherins in postnatal mouse brains. Mol. Cell. Neurosci. 9, 433-447.
64. Tabata, H. and Nakajima, K. (2001). Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103, 865-872.
65. Taghert, P. H., Bastiani, M. J., Ho, R. K. and Goodman, C. S. (1982). Guidance of pioneer growth cones: filopodial contacts and coupling revealed with an antibody to Lucifer Yellow. Dev. Biol. 94, 391-399.
66. Takeuchi, T., Misaki, A., Liang, S.-B., Tachibana, A., Hayashi, N., Sonobe, H. and Ohtsuki, Y. (2000). Expression of T-cadherin (CDH13, H-Cadherin) in human brain and its characteristics as a negative growth regulator of epidermal growth factor in neuroblastoma cells. J. Neurochem. 74, 1489-1497.
67. Treubert-Zimmermann, U., Heyers, D. and Redies, C. (2002). Targeting axons to specific fiber tracts in vivo by altering cadherin expression. J. Neurosci. 22, 7617-7626.
68. Van Vactor, D. (1998). Adhesion and signaling in axonal fasciculation. Curr. Opin. Neurobiol. 8, 80-86.
69. Vestal, D. J. and Ranscht, B. (1992). Glycosyl phosphatidylinositol-anchored T- cadherin mediates calcium-dependent, homophilic cell adhesion. J. Cell Biol. 119, 451-461.
70. Wang, L. and Marquardt, T. (2013). What axons tell each other: axon-axon signaling in nerve and circuit assembly. Curr. Opin. Neurobiol. 23, 974-982.
71. Weiner, J. A., Koo, S. J., Nicolas, S., Fraboulet, S., Pfaff, S. L., Pourquie, O. and Sanes, J. R. (2004). Axon fasciculation defects and retinal dysplasias in mice lacking the immunoglobulin superfamily adhesion molecule BEN/ALCAM/SC1. Mol. Cell. Neurosci. 27, 59-69.
72. Wiencken-Barger, A. E., Mavity-Hudson, J., Bartsch, U., Schachner, M. and Casagrande, V. A. (2004). The role of L1 in axon pathfinding and fasciculation. Cereb. Cortex 14, 121-131.
73. Wolfer, D. P., Henehan-Beatty, A., Stoeckli, E. T., Sonderegger, P. and Lipp, H.- P. (1994). Distribution of TAG-1/axonin-1 in fibre tracts and migratory streams of the developing mouse nervous system. J. Comp. Neurol. 345, 1-32
74. Woodward, W. R., Chiaia, N., Teyler, T. J., Leong, L. and Coull, B. M. (1990). Organization of cortical afferent and efferent pathways in the white matter of the rat visual system. Neuroscience 36, 393-401.
75. Zhao, H., Maruyama, T., Hattori, Y., Sugo, N., Takamatsu, H., Kumanogoh, A., Shirasaki, R. and Yamamoto, N. (2011). A molecular mechanism that regulates medially oriented axonal growth of upper layer neurons in the developing neocortex. J. Comp. Neurol. 519, 834-848.
76. Zhong, Y., Takemoto, M., Fukuda, T., Hattori, Y., Murakami, F., Nakajima, D., Nakayama, M. and Yamamoto, N. (2004). Identification of the genes that are expressed in the upper layers of the neocortex. Cereb. Cortex 14, 1144-1152.