Transcriptional regulation of vertebrate axon guidance and synapse formation

Nature Reviews Neuroscience

Volumn 8, Issue 5, 2007, Pages 331-340

  Polleux, Franck ^a   Ince Dunn, Gulayse ^b   Ghosh, Anirvan ^c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; BONE MORPHOGENETIC PROTEIN; EPHRIN A5; EPHRIN RECEPTOR A3; EPHRIN RECEPTOR A4; EPHRIN RECEPTOR B1; FIBROBLAST GROWTH FACTOR 8; FORKHEAD TRANSCRIPTION FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; HOMEODOMAIN PROTEIN; LIM HOMEOBOX 1 PROTEIN; LIM HOMEODOMAIN TRANSCRIPTION FACTOR ISLET 2; NEUROPILIN 1; NEUROTRANSMITTER; PROTEIN; PROTEIN VAX2; RETINOIC ACID; SEMAPHORIN 3A; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ER81; TRANSCRIPTION FACTOR NEUROGENIC DIFFERENTIATION D2; TRANSCRIPTION FACTOR NEUROGENIN2; TRANSCRIPTION FACTOR PAX2; UNCLASSIFIED DRUG; ZIC2 PROTEIN;

BINOCULAR VISION; BRAIN CORTEX; BRAIN STEM; CHICK; DEPHOSPHORYLATION; EXCITATORY POSTSYNAPTIC POTENTIAL; EYE DEVELOPMENT; FLUORESCENCE ACTIVATED CELL SORTER; GENE EXPRESSION; INVERTEBRATE; KNOCKOUT MOUSE; MOTONEURON; MOUSE STRAIN; NERVE ENDING; NERVE FIBER; NERVOUS SYSTEM; NEUROTRANSMISSION; NONHUMAN; OPTIC CHIASM; OPTIC TECTUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA GANGLION CELL; REVIEW; SPINAL CORD; SYNAPSE; SYNAPTOGENESIS; TELENCEPHALON; THALAMUS; TOPOGRAPHY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VERTEBRATE; XENOPUS;

ANIMALS; AXONS; MODELS, BIOLOGICAL; NEURONS; ORGANOGENESIS; SYNAPSES; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; VERTEBRATES;

VERTEBRATA;

EID: 34247516542     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn2118     Document Type: Review

References (91)

1. Tessier-Lavigne M. & Goodman, C. S. The molecular biology of axon guidance. Science 274, 1123-1133 (1996).
2. Dickson, B. J. Molecular mechanisms of axon guidance. Science 298, 1959-1964 (2002).
3. Huber, A. B., Kolodkin, A. L., Ginty, D. D. & Cloutier, J. F. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu. Rev. Neurosci. 26, 509-563 (2003).
4. Herrera, E. et al. Zic2 patterns binocular vision by specifying the uncrossed retinal projection. Cell 114, 545-557 (2003).
5. Pak, W., Hindges, R., Lim, Y. S., Pfaff, S. L. & O'Leary, D. D. Magnitude of binocular vision controlled by islet-2 repression of a genetic program that specifies laterality of retinal axon pathfinding. Cell 119, 567-578 (2004). Together with reference 4, these were the first two papers to show transcriptional control of retinal axon guidance at the optic chiasm.
6. Nagai, T. et al. The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. Dev. Biol. 182, 299-313 (1997).
7. Nagai, T. et al. Zic2 regulates the kinetics of neurulation. Proc. Natl Acad. Sci. USA 97, 1618-1623 (2000).
8. Williams, S. E. et al. Ephrin-B2 and EphB1 mediate retinal axon divergence at the optic chiasm. Neuron 39, 919-935 (2003).
9. Flanagan, J. G. & Vanderhaeghen, P. The ephrins and Eph receptors in neural development. Annu. Rev. Neurosci. 21, 309-345 (1998).
10. McLaughlin, T., Hindges, R. & O'Leary, D. D. Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr. Opin. Neurobiol. 13, 57-69 (2003).
11. Schulte, D., Furukawa, T., Peters, M. A., Kozak, C. A. & Cepko, C. L. Misexpression of the Emx-related homeobox genes cVax and mVax2 ventralizes the retina and perturbs the retinotectal map. Neuron 24, 541-553 (1999).
12. Mui, S. H., Hindges, R., O'Leary, D. D., Lemke, G. & Bertuzzi, S. The homeodomain protein Vax2 patterns the dorsoventral and nasotemporal axes of the eye. Development 129, 797-804 (2002).
13. Barbieri, A. M. et al. Vax2 inactivation in mouse determines alteration of the eye dorsal-ventral axis, misrouting of the optic fibres and eye coloboma. Development 129, 805-813 (2002).
14. Koshiba-Takeuchi, K. et al. Tbx5 and the retinotectum projection. Science 287, 134-137 (2000).
15. Wagner, E., McCaffery, P. & Drager, U. C. Retinoic acid in the formation of the dorsoventral retina and its central projections. Dev. Biol. 222, 460-470 (2000).
16. Zhao, S., Chen, Q., Hung, F. C. & Overbeek, P. A. BMP signaling is required for development of the ciliary body. Development 129, 4435-4217 (2002).
17. Sen, J., Harpavat, S., Peters, M. A. & Cepko, C. L. Retinoic acid regulates the expression of dorsoventral topographic guidance molecules in the chick retina. Development 132, 5147-5159 (2005).
18. Sakuta, H. et al. Ventroptin: a BMP-4 antagonist expressed in a double-gradient pattern in the retina. Science 293, 111-115 (2001).
19. Lupo, G. et al. Dorsoventral patterning of the Xenopus eye: a collaboration of Retinoid, Hedgehog and FGF receptor signaling. Development 132, 1737-1748 (2005).
20. Mann, F., Ray, S., Harris, W. & Holt, C. Topographic mapping in dorsoventral axis of the Xenopus retinotectal system depends on signaling through ephrin-B ligands. Neuron 35, 461-473 (2002).
21. Yuasa, J., Hirano, S., Yamagata, M. & Noda, M. Visual projection map specified by topographic expression of transcription factors in the retina. Nature 382, 632-635 (1996).
22. Takahashi, H., Shintani, T., Sakuta, H. & Noda, M. CBF1 controls the retinotectal topographical map along the anteroposterior axis through multiple mechanisms. Development 130, 5203-5215 (2003).
23. Herrera, E. et al. Foxd1 is required for proper formation of the optic chiasm. Development 131, 5727-5739 (2004).
24. Pratt, T., Tian, N. M., Simpson, T. I., Mason, J. O. & Price, D. J. The winged helix transcription factor Foxg1 facilitates retinal ganglion cell axon crossing of the ventral midline in the mouse. Development 131, 3773-3784 (2004).
25. Garel, S., Yun, K., Grosschedl, R. & Rubenstein, J. L. The early topography of thalamocortical projections is shifted in Ebf1 and Dlx1/2 mutant mice. Development 129, 5621-5634 (2002).
26. Garel, S. & Rubenstein, J. L. Intermediate targets in formation of topographic projections: inputs from the thalamocortical system. Trends Neurosci. 27, 533-539 (2004).
27. Garel, S., Huffman, K. J. & Rubenstein, J. L. Molecular regionalization of the neocortex is disrupted in Fgf8 hypomorphic mutants. Development 130, 1903-1914 (2003).
28. Vanderhaeghen, P. & Polleux, F. Developmental mechanisms patterning thalamocortical projections: intrinsic, extrinsic and in between. Trends Neurosci. 27, 384-391 (2004).
29. Seibt, J. et al. Neurogenin2 specifies the connectivity of thalamic neurons by controlling axon responsiveness to intermediate target cues. Neuron 39, 439-452 (2003).
30. Nakagawa, Y. & O'Leary, D. D. Combinatorial expression patterns of LIM-homeodomain and other regulatory genes parcellate developing thalamus. J. Neurosci. 21, 2711-2725 (2001).
31. Caviness, V. S. Jr & Frost, D. O. Tangential organization of thalamic projections to the neocortex in the mouse. J. Comp. Neurol. 194, 335-367 (1980).
32. Crandall, J. E. & Caviness, V. S. Jr. Thalamocortical connections in newborn mice. J. Comp. Neurol. 228, 542-556 (1984).
33. Hohl-Abrahao, J. C. & Creutzfeldt, O. D. Topographical mapping of the thalamocortical projections in rodents and comparison with that in primates. Exp. Brain Res. 87, 283-294 (1991).
34. Dufour, A. et al. Area specificity and topography of thalamocortical projections are controlled by ephrin/Eph genes. Neuron 39, 453-465 (2003).
35. Ince-Dunn, G. et al. Regulation of thalamocortical patterning and synaptic maturation by NeuroD2. Neuron 49, 683-695 (2006).
36. Kashani, A. H. et al. Calcium activation of the LMO4 transcription complex and its role in the patterning of thalamocortical connections. J. Neurosci. 26, 8398-8408 (2006). Together with reference 35, these were the first two papers to show transcription-factor control of barrel-cortex connectivity.
37. Aizawa, H. et al. Dendrite development regulated by CREST, a calcium-regulated transcriptional activator. Science 303, 197-202 (2004).
38. Senft, S. L. & Woolsey, T. A. Growth of thalamic afferents into mouse barrel cortex. Cereb. Cortex 1, 308-335 (1991).
39. Woolsey, T. A. & Van der Loos, H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 17, 205-242 (1970).
40. Iwasato, T. et al. NMDA receptor-dependent refinement of somatotopic maps. Neuron 19, 1201-1210 (1997).
41. Iwasato, T. et al. Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 406, 726-731 (2000).
42. Hannan, A. J. PLC-β1, activated via mGluRs, mediates activity-dependent differentiation in cerebral cortex. Nature Neurosci. 4, 282-288 (2001).
43. Koester, S. E. & O'Leary, D. D. Development of projection neurons of the mammalian cerebral cortex. Prog. Brain Res. 102, 207-215 (1994).
44. O'Leary, D. D. & Koester, S. E. Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex. Neuron 10, 991-1006 (1993).
45. Arlotta, P. et al. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45, 207-221 (2005). Transcriptional profiling of identified subpopulations of pyramidal neurons during development demonstrated that CTIP2 is specifically required for proper development of corticospinal projections.
46. Chen, B., Schaevitz, L. R. & McConnell, S. K. Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc. Natl Acad. Sci. USA 102, 17184-17189 (2005).
47. Chen, J. G., Rasin, M. R., Kwan, K. Y. & Sestan, N. Zfp312 is required for subcortical axonal projections and dendritic morphology of deep-layer pyramidal neurons of the cerebral cortex. Proc. Natl Acad. Sci. USA 102, 17792-17797 (2005).
48. Hirata, T. et al. Zinc finger gene fez-like functions in the formation of subplate neurons and thalamocortical axons. Dev. Dyn. 230, 546-556 (2004).
49. Molyneaux, B. J., Arlotta, P., Hirata, T., Hibi, M. & Macklis, J. D. Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 47, 817-831 (2005).
50. Hevner, R. F. et al. Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29, 353-366 (2001).
51. Shirasaki, R. & Pfaff, S. L. Transcriptional codes and the control of neuronal identity. Annu. Rev. Neurosci. 25, 251-281 (2002).
52. Pfaff, S. L., Mendelsohn, M., Stewart, C. L., Edlund, T., Jessell, T. M. Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84, 309-320 (1996).
53. Hollyday M. Organization of motor pools in the chick lumbar lateral motor column. J. Comp. Neurol. 194, 143-170 (1980).
54. Lance-Jones, C. & Landmesser, L. Pathway selection by embryonic chick motoneurons in an experimentally altered environment. Proc. R. Soc. Lond. B Biol. Sci. 214, 19-52 (1981).
55. Landmesser L. The distribution of motoneurones supplying chick hind limb muscles. J. Physiol. 284, 371-389 (1978).
56. Landmesser L. The relationship of intramuscular nerve branching and synaptogenesis to motoneuron survival. J. Neurobiol. 23, 1131-1139 (1992).
57. Briscoe, J., Pierani, A., Jessell, T. M. & Ericson, J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101, 435-445 (2000).
58. Sharma, K., Leonard, A. E., Lettieri, K. & Pfaff, S. L. Genetic and epigenetic mechanisms contribute to motor neuron pathfinding. Nature 406, 515-519 (2000).
59. Tsuchida, T. et al. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-970 (1994).
60. Dasen, J. S., Tice, B. C., Brenner-Morton, S. & Jessell, T. M. A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123, 477-491 (2005).
61. Kania, A., Johnson, R. L. & Jessell, T. M. Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell 102, 161-173 (2000).
62. Hobert, O., D'Alberti, T., Liu, Y. & Ruvkun, G. Control of neural development and function in a thermoregulatory network by the LIM homeobox gene lin-11. J. Neurosci. 18, 2084-2096 (1998).
63. Thor, S., Andersson, S. G., Tomlinson, A. & Thomas, J. B. A LIM-homeodomain combinatorial code for motorneuron pathway selection. Nature 397, 76-80 (1999).
64. Iwamasa, H. et al. Expression of Eph receptor tyrosine kinases and their ligands in chick embryonic motor neurons and hindlimb muscles. Dev. Growth Differ. 41, 685-698 (1999).
65. Helmbacher, F., Schneider-Maunoury, S., Topilko, P., Tiret, L. & Charnay, P. Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons. Development 127, 3313-3324 (2000).
66. Eberhart, J. et al. Expression of EphA4, ephrin-A2 and ephrin-A5 during axon outgrowth to the hindlimb indicates potential roles in pathfinding. Dev. Neurosci. 22, 237-250 (2000).
67. Eberhart, J. et al. 2004. Ephrin-A5 exerts positive or inhibitory effects on distinct subsets of EphA4-positive motor neurons. J. Neurosci. 24, 1070-1078
68. Kania, A., Jessell, T. M. Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 38, 581-596 (2003).
69. Huber, A. B. et al. Distinct roles for secreted semaphorin signaling in spinal motor axon guidance. Neuron 48, 949-964 (2005).
70. Shirasaki, R., Lewcock, J. W., Lettieri, K. & Pfaff, S. L. FGF as a target-derived chemoattractant for developing motor axons genetically programmed by the LIM code. Neuron 50, 841-853 (2006).
71. Arber, S., Ladle, D. R., Lin, J. H., Frank, E. & Jessell, T. M. ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 101, 485-498 (2000).
72. Lin, J. H. et al. Functionally related motor neuron pool and muscle sensory afferent subtypes defined by coordinate ETS gene expression. Cell 95, 393-407 (1998).
73. Livet, J. et al. ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools. Neuron 35, 877-892 (2002).
74. Haase, G. et al. GDNF acts through PEA3 to regulate cell body positioning and muscle innervation of specific motor neuron pools. Neuron 35, 893-905 (2002).
75. Patel, T. D. et al. Peripheral NT3 signaling is required for ETS protein expression and central patterning of proprioceptive sensory afferents. Neuron 38, 403-416 (2003).
76. Vrieseling, E. & Arber, S. Target-induced transcriptional control of dendritic patterning and connectivity in motor neurons by ETS gene Pea3. Cell 127, 1439-1452 (2006).
77. Polleux, F., Morrow, T. & Ghosh, A. Semaphorin 3A is a chemoattractant for developing cortical dendrites. Nature 404, 567-573 (2000).
78. McKinsey, T. A., Zhang, C. L. & Olson, E. N. MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem. Sci. 27, 40-47 (2002).
79. Flavell, S. W. et al. Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311, 1008-1012 (2006). Uncovers the molecular mechanisms by which MEF2A/D regulates the numbers of excitatory synapses in cortical neurons.
80. Mao, Z., Bonni, A., Xia, F., Nadal-Vicens, M. & Greenberg, M. E. Neuronal activity-dependent cell survival mediated by transcription factor MEF2. Science 286, 785-790 (1999).
81. Shalizi, A. et al. A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311, 1012-1017 (2006).
82. Salama-Cohen, P., Arevalo, M. A., Grantyn, R. & Rodriguez-Tebar, A. Notch and NGF/p75NTR control dendrite morphology and the balance of excitatory/inhibitory synaptic input to hippocampal neurones through Neurogenin 3. J. Neurochem. 97, 1269-1278 (2006).
83. Redmond, L., Kashani, A. & Ghosh, A. Calcium regulation of dendritic growth via Cam kinase IV and CREB-mediated transcription. Neuron 34, 999-1010 (2002).
84. Marie, H., Morishita, W., Yu, X., Calakos, N. & Malenka, R. C. Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45, 741-752 (2005).
85. Crair, M. C. & Malenka, R. C. A critical period for long-term potentiation at thalamocortical synapses. Nature 375, 325-328 (1995).
86. Feldman, D. E., Nicoll, R. A., Malenka, R. C. & Isaac, J. T. Long-term depression at thalamocortical synapses in developing rat somatosensory cortex. Neuron 21, 347-357 (1998).
87. Isaac, J. T., Crair, M. C., Nicoll, R. A. & Malenka, R. C. Silent synapses during development of thalamocortical inputs. Neuron 18, 269-280 (1997).
88. Gray, P. A. et al. Mouse brain organization revealed through direct genome scale transcription factor expression analysis. Science 306, 2255-2257 (2004).
89. Magdaleno S, BGEM: an in situ hybridization database of gene expression in the embryonic and adult mouse nervous system. PLoS Biol. 4, e86 (2006).
90. Lein E. et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445,168-176 (2007).
91. Sugino, K. et al. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nature Neurosci. 9, 99-107 (2006).