Defects in thalamocortical axon pathfinding correlate with altered cell domains in Mash-1-deficient mice

Development

Volumn 126, Issue 9, 1999, Pages 1903-1916

  Tuttle, Rebecca ^a   Nakagawa, Yasushi ^a   Johnson, Jane E ^b   O'Leary, Dennis D M ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Axon guidance; Dorsal thalamus; Forebrain patterning; Globus pallidus; Hypothalamus; L1; Netrin 1; Nkx 2.1; Nkx 2.2; Pax 6; RPTP ; Telencephalon; Transcription factors; ventral thalamus

Indexed keywords

TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HYPOTHALAMUS; MOUSE; MOUSE MUTANT; NEOCORTEX; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TELENCEPHALON; THALAMOCORTICAL TRACT; THALAMUS;

AFFERENT PATHWAYS; ANIMALS; AXONS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CEREBRAL CORTEX; CROSSES, GENETIC; DNA-BINDING PROTEINS; EFFERENT PATHWAYS; EMBRYONIC AND FETAL DEVELOPMENT; HELIX-LOOP-HELIX MOTIFS; HETEROZYGOTE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROSENCEPHALON; TELENCEPHALON; THALAMUS; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 0032967746     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (71)

1. Angevine, J. B., Jr. (1970). Time of neuron origin in the diencephalon of the mouse. An autoradiographic study. J. Comp. Neurol. 139, 129-187.
2. Ba-Charvet, K. T., von Boxberg, Y., Guazzi, S., Boncinelli, E. and Godement, P. (1998). A potential role for the OTX2 homeoprotein in creating early 'highways' for axon extension in the rostral brain. Development 125, 4273-4282.
3. Bicknese, A. R., Sheppard, A. M., O'Leary, D. D. M. 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.
4. Braisted, J. B., Tuttle, R. and O'Leary, D. D. M. (1999). Thalamocortical axons are influenced by chemorepellent and chemoattractant activities localized to decision points along their path. Dev. Biol., In Press.
5. Bray, D., Wood, P. and Bunge, R. P. (1980). Selective fasciculation of nerve fibres in culture. Exp. Cell Res. 130, 241-250.
6. Bruckner, K., Pasquale, E. B. and Klein, R. (1997). Tyrosine phosphorylation of transmembrane ligands for Eph receptors. Science 275, 1640-1643.
7. Brummendorf, T., Kenwrick, S. and Rathjen, F. G. (1998). Neural cell recognition molecule L1: from cell biology to human hereditary brain malformations. Curr. Opin. Neurobiol. 8, 87-97.
8. Butler, H. and Juurlink, B. H. J. (1987). An Atlas for Staging Mammalian and Chick Embryos. Boca Raton: CRC Press.
9. Campuzano, S. and Modolell, J. (1992). Patterning of the Drosophila nervous system: the achaete-scute gene complex. Trends Genet. 8, 202-208.
10. Cau, E., Gradwohl, G., Fode, C. and Guillemot, F. (1997). Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors. Development 124, 1611-1621.
11. Desai, C. J., Gindhart, J. G., Jr., Goldstein, L. S. and Zinn, K. (1996). Receptor tyrosine phosphatases are required for motor axon guidance in the Drosophila embryo. Cell 84, 599-609.
12. Emerling, D. E. and Lander, A. D. (1996). Inhibitors and promoters of thalamic neuron adhesion and outgrowth in embryonic neocortex: functional association with chondroitin sulfate. Neuron 17, 1089-1100.
13. Figdor, M. C. and Stern, C. D. (1993). Segmental organization of embryonic diencephalon. Nature 363, 630-634.
14. Friedman, G. C. and O'Leary, D. D. M. (1996). Retroviral misexpression of engrailed genes in the chick optic tectum perturbs the topographic targeting of retinal axons. J. Neurosci. 16, 5498-5509.
15. 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.
16. Guazzi, S., Price, M., De Felice, M., Damante, G., Mattei, M. G. and Di Lauro, R. (1990). Thyroid nuclear factor 1 (TTF-1) contains a homeodomain and displays a novel DNA binding specificity. EMBO J. 9, 3631-3639.
17. Guillemot, F. and Joyner, A. L. (1993) Dynamic expression of the murine Achaete-Scute homologue Mash-1 in the developing nervous system. Mech. Dev. 42, 171-185.
18. Guillemot, F., Lo, L. C., Johnson, J. E., Auerbach, A., Anderson, D. J. and Joyner, A. L. (1993). Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomie neurons. Cell 75, 463-476.
19. Henkemeyer, M., Orioli, D., Henderson, J. T., Saxton, T. M., Roder, J., Pawson, T. and Klein, R. (1996). Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 86, 35-46.
20. Hirsch, M. R., Tiveron, M. C., Guillemot, F., Brunet, J. F. and Goridis, C. (1998). Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development 125, 599-608.
21. Holland, S. J., Gale, N. W., Mbamalu, G., Yancopoulos, G. D., Henkemeyer, M. and Pawson, T. (1996). Bidirectional signalling through the EPH-family receptor Nuk and its transmembrane ligands. Nature 383, 722-725.
22. Holland, S. J., Peles, E., Pawson, T. and Schlessinger, J. (1998). Cell-contact-dependent signalling in axon growth and guidance: Eph receptor tyrosine kinases and receptor protein tyrosine phosphatase beta. Curr. Opin. Neurobiol. 8, 117-127.
23. Itasaki, N. and Nakamura, H. (1996). A role for gradient en expression in positional specification on the optic tectum. Neuron 16, 55-62.
24. Jan, Y. N. and Jan, L. Y. (1994). Neuronal cell fate specification in Drosophila. Curr. Opin. Neurobiol. 4, 8-13.
25. Johnson, J. E., Birren, S. J. and Anderson, D. J. (1990). Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature 346, 858-861.
26. Jones, E. G. (1985). The Thalamus. New York: Plenum Press.
27. Kamiguchi, H. and Lemmon, V. (1997). Neural cell adhesion molecule L1: signaling pathways and growth cone motility. J. Neurosci. Res. 49, 1-8.
28. Kennedy, T. E., Serafini, T., de la Torre, J. R. and Tessier-Lavigne, M. (1994). Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78, 425-435.
29. Kitamura, K., Miura, H., Yanazawa, M., Miyashita, T. and Kato, K. (1997). Expression patterns of Brx1 (Rieg gene). Sonic hedgehog, Nkx2.2, Dlx1 and Arx during zona limitans intrathalamica and embryonic ventral lateral geniculate nuclear formation. Mech. Dev. 67, 83-96.
30. Kohtz, J. D., Baker, D. P., Corte, G. and Fishell, G. (1998). Regionalization within the mammalian telencephalon is mediated by changes in responsiveness to Sonic Hedgehog. Development 125, 5079-5089.
31. Krauss, S., Johansen, T., Korzh, V. and Fjose, A. (1991). Expression pattern of zebrafish pax genes suggests a role in early brain regionalization. Nature 353, 267-270.
32. Krueger, N. X., Streuli, M. and Saito, H. (1990). Structural diversity and evolution of human receptor-like protein tyrosine phosphatases. EMBO J. 9, 3241-3252.
33. Krueger, N. X., Van Vactor, D., Wan, H. I., Gelbart, W. M., Goodman, C. S. and Saito, H. (1996). The transmembrane tyrosine phosphatase DLAR controls motor axon guidance in Drosophila. Cell 84, 611-622.
34. Lauderdale, J. D., Pasquali, S. K., Fazel, R., van Eeden, F. J., Schauerte, H. E., Haffter, P. and Kuwada, J. Y. (1998). Regulation of netrin-1a expression by hedgehog proteins. Molec. Cell Neurosci. 11, 194-205.
35. Lazzaro, D., Price, M., de Felice, M. and Di Lauro, R. (1991). The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113, 1093-1104.
36. Lo, L.-C., Johnson, J. E., Wuenschell, C. W., Saito, T. and Anderson, D. J. (1991). Mammalian achaete-scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes & Development 5, 1524-1537.
37. Logan, C., Wizenmann, A., Drescher, U., Monschau, B., Bonhoeffer, F. and Lumsden, A. (1996). Rostral optic tectum acquires caudal characteristics following ectopic engrailed expression. Curr. Biol. 6, 1006-1014.
38. Lumsden, A. and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 274, 1109-1115.
39. Macdonald, R., Xu, Q., Barth, K. A., Mikkola, I., Holder, N., Fjose, A., Krauss, S. and Wilson, S. W. (1994). Regulatory gene expression boundaries demarcate sites of neuronal differentiation in the embryonic zebrafish forebrain. Neuron 13, 1039-1053.
40. Mastick, G. S., Davis, N. M., Andrew, G. L., Easter, S. S. (1997). Pax-6 functions in boundary formation and axon guidance in the embryonic mouse forebrain. Development 124, 1985-97.
41. Métin, C., Deléglise, D., Serafini, T., Kennedy, T. E. and Tessier-Lavigne, M. (1997). A role for netrin-1 in the guidance of cortical efferents. Development 124, 5063-5074.
42. Métin, C. and Godement, P. (1996). The ganglionic eminence may be an intermediate target for corticofugal and thalamocortical axons. J. Neurosci. 16, 3219-3235.
43. Mitchell, K. J., Doyle, J. L., Serafini, T., Kennedy, T. E., Tessier-Lavigne, M., Goodman, C. S. and Dickson, B. J. (1996). Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 17, 203-215.
44. Mitrofanis, J. and Guillery, R. W. (1993). New views of the thalamic reticular nucleus in the adult and the developing brain. Trends Neurosci. 16, 240-245.
45. Mizuno, K., Hasegawa, K., Katagiri, T., Ogimoto, M., Ichikawa, T. and Yakura, H. (1993). MPTP delta, a putative murine homolog of HPTP delta, is expressed in specialized regions of the brain and in the B-cell lineage. Mol. Cell Biol. 13, 5513-5523.
46. Molnar, Z., Adams, R. and Blakemore, C. (1998). Mechanisms underlying the early establishment of thalamocortical connections in the rat. J. Neurosci. 18, 5723-5745.
47. Olsson, M., Campbell, K. and Turnbull, D. H. (1997). Specification of mouse telencephalic and mid-hindbrain progenitors following heterotopic ultrasound-guided embryonic transplantation. Neuron 19, 761-772.
48. Orioli, D., Henkemeyer, M., Lemke, G., Klein, R., and Pawson, T. (1996). Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation. EMBO J. 15, 6035-6049.
49. Ozaki, H. S. and Wahlsten, D. (1993). Cortical axon trajectories and growth cone morphologies in fetuses of acallosal mouse strains. J. Comp. Neurol. 336, 595-604.
50. Papalopulu, N. (1995). Regionalization of the forebrain from neural plate to neural tube. Perspect. Dev. Neurobiol. 3, 39-52.
51. Peles, E., Nativ, M., Campbell, P. L., Sakurai, T., Martinez, R., Lev, S., Clary, D. O., Schilling, J., Barnea, G., Plowman, G. D., et al. (1995). The carbonic anhydrase domain of receptor tyrosine phosphatase beta is a functional ligand for the axonal cell recognition molecule contactin. Cell 82, 251-260.
52. Porteus, M. H., Bulfone, A., Liu, J. K., Puelles, L., Lo, L. C. and Rubenstein, J. L. (1994). DLX-2, MASH-1, and MAP-2 expression and bromodeoxyuridine incorporation define molecularly distinct cell populations in the embryonic mouse forebrain. J. Neurosci. 14, 6370-6383.
53. Price, M., Lazzaro, D., Pohl, T., Mattei, M. G., Ruther, U., Olivo, J. C., Duboule, D. and Di Lauro, R. (1992). Regional expression of the homeobox gene Nkx-2.2 in the developing mammalian forebrain. Neuron 8, 241-255.
54. Puelles, L. (1995). A segmental morphological paradigm for understanding vertebrate forebrains. Brain Behav. Evol. 46, 319-337.
55. Puelles, L. and Rubenstein, J. L. (1993). Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci. 16, 472-479.
56. Ricardo, J. A. (1981). Efferent connections of the subthalamic region in the rat. II. The zona incerta. Brain Res. 214, 43-60.
57. Richards, L. R., Koester, S. E., Tuttle, R. and O'Leary, D.D.M. (1997). Directed growth of early cortical axons is influencedby a chemoattractant released from an intermediate target. J. Neurosci. 17, 2445-2458.
58. Serafini, T., Colamarino, S. A., Leonardo, E. D., Wang, H., Beddington, R., Skarnes, W. C. and Tessier-Lavigne, M. (1996). Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87, 1001-1014.
59. Serafini, T., Kennedy, T. E., Galko, M. J., Mirzayan, C., Jessell, T. M. and Tessier-Lavigne, M. (1994). The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424.
60. Shigetani, Y., Funahashi, J. I. and Nakamura, H. (1997). En-2 regulates the expression of the ligands for Eph type tyrosine kinases in chick embryonic lectum. Neurosci. Res. 27, 211-217.
61. Shimamura, K., Hartigan, D. J., Martinez, S., Puelles, L. and Rubenstein, J. L. (1995). Longitudinal organization of the anterior neural plate and neural tube. Development 121, 3923-3933.
62. Sommer, L., Rao, M. and Anderson, D. J. (1997). RPTP delta and the novel protein tyrosine phosphatase RPTP psi are expressed in restricted regions of the developing central nervous system. Dev. Dynam. 208, 48-61.
63. Sommer, L., Shah, N., Rao, M. and Anderson, D. J. (1995). The cellular function of MASH1 in autonomie neurogenesis. Neuron 15, 1245-1258.
64. Stoykova, A., Fritsch, R., Walther, C. and Gruss, P. (1996). Forebrain patterning defects in Small eye mutant mice. Development 122, 3453-3465.
65. Tessier-Lavigne, M. and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
66. Tuttle, R., Braisted, J. E., Richards, L. J. and O'Leary, D. D. M. (1998). Retinal axon guidance by region-specific cues in diencephalon. Development 125, 791-801.
67. Tuttle, R., Schlaggar, B. L., Braisted, J. E. and O'Leary, D. D. M. (1995). Maturation-dependent upregulation of growth-promoting molecules in developing cortical plate controls thalamic and cortical neurite growth. J. Neurosci. 15, 3039-3052.
68. van der Kooy, D. and Carter, D. A. (1981). The organization of the efferent projections and striatal afferents of the entopeduncular nucleus and adjacent areas in the rat. Brain Res. 211, 15-36.
69. Verma-Kurvari, S., Savage, T., Gowan, K. and Johnson, J. E. (1996). Lineage-specific regulation of the neural differentiation gene MASH1. Dev. Biol. 180, 605-617.
70. Walther, C. and Gruss, P. (1991). Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435-1449.
71. Wang, J. and Bixby, J. L. (1998). The extracellular domain of tyrosine phosphatase delta is adhesive for neurons and promotes neurite outgrowth in vitro. Soc. Neurosci. Abstr. 24, 1285.