Astrocyte-encoded positional cues maintain sensorimotor circuit integrity

Nature

Volumn 509, Issue 7499, 2014, Pages 189-194

  Molofsky, Anna V ^a   Kelley, Kevin W ^a,b   Tsai, Hui Hsin ^a,b   Redmond, Stephanie A ^a,b   Chang, Sandra M ^a   Madireddy, Lohith ^b   Chan, Jonah R ^b   Baranzini, Sergio E ^b   Ullian, Erik M ^b   Rowitch, David H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN TYROSINE KINASE A; SEMAPHORIN 3A;

NERVOUS SYSTEM; NEUROLOGY; SENSORY SYSTEM;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; BRAIN REGION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; GENE; MOUSE; NERVE CELL NETWORK; NERVE FIBER; NERVE PROJECTION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SEMA3A GENE; SENSORIMOTOR FUNCTION; SENSORY NERVE; SPINAL CORD; SYNAPSE;

ANIMALS; ASTROCYTES; AXONS; CELL POLARITY; CELL SURVIVAL; HUMANS; MICE; MOTOR NEURONS; NEURAL PATHWAYS; SEMAPHORIN-3A; SENSORY RECEPTOR CELLS; SPINAL CORD; SYNAPSES;

EID: 84899946489     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13161     Document Type: Article

References (44)

1. Clarke, L. E. & Barres, B. A. Emerging roles of astrocytes in neural circuitdevelopment. Nature Rev. Neurosci. 14, 311-321 (2013).
2. Tsai, H.-H. et al. Regional astrocyte allocation regulates CNS synaptogenesis andrepair. Science 337, 358-362 (2012).
3. Hochstim, C., Deneen, B., Lukaszewicz, A., Zhou, Q. & Anderson, D. J. Identificationof positionally distinct astrocyte subtypes whose identities are specified by ahomeodomain code. Cell 133, 510-522 (2008).
4. Muroyama, Y., Fujiwara, Y., Orkin, S. H. & Rowitch, D. H. Specification of astrocytesby bHLH protein SCL in a restricted region of the neural tube. Nature 438,360-363 (2005).
5. Rowitch, D. H. & Kriegstein, A. R. Developmental genetics of vertebrate glial-cellspecification. Nature 468, 214-222 (2010).
6. Ge, W.-P., Miyawaki, A., Gage, F. H., Jan, Y.-N. & Jan, L. Y. Local generation of glia is amajor astrocyte source in postnatal cortex. Nature 484, 376-380 (2012).
7. Tien, A.-C. et al. Regulated temporal-spatial astrocyte precursor cell proliferationinvolves BRAF signalling in mammalian spinal cord. Development 139,2477-2487 (2012).
8. Magavi, S., Friedmann, D., Banks, G., Stolfi, A. & Lois, C. Coincident generation ofpyramidal neurons and protoplasmic astrocytes in neocortical columns.J. Neurosci. 32, 4762-4772 (2012).
9. Jessell, T. M. Neuronal specification in the spinal cord: inductive signals andtranscriptional codes. Nature Rev. Genet. 1, 20-29 (2000).
10. Friese, A. et al. Gamma and alpha motor neurons distinguished by expression oftranscription factor Err3. Proc. Natl Acad. Sci. USA 106, 13588-13593 (2009).
11. Arber, S. Motor circuits in action: specification, connectivity, and function. Neuron74, 975-989 (2012).
12. Dasen, J. S.& Jessell, T. M. Hox networks and the origins ofmotor neuron diversity.Curr. Top. Dev. Biol. 88, 169-200 (2009).
13. Sürmeli, G., Akay, T., Ippolito, G. C., Tucker, P. W. & Jessell, T. M. Patterns of spinalsensory-motor connectivity prescribed by a dorsoventral positional template. Cell147, 653-665 (2011).
14. Messersmith, E. K. et al. Semaphorin III can function as a selective chemorepellentto pattern sensory projections in the spinal cord. Neuron 14, 949-959 (1995).
15. Kolodkin, A. L. et al. Neuropilin is a semaphorin III receptor. Cell 90, 753-762(1997).
16. Pasterkamp, R. J. & Giger, R. J. Semaphorin function in neural plasticity anddisease. Curr. Opin. Neurobiol. 19, 263-274 (2009).
17. Cahoy, J. D. et al. A transcriptome database for astrocytes, neurons, andoligodendrocytes: a new resource for understanding brain development andfunction. J. Neurosci. 28, 264-278 (2008).
18. Molofsky, A. V. et al. Expression profiling of Aldh1l1-precursors in the developingspinal cord reveals glial lineage-specific genes and direct Sox9-Nfe2l1interactions. Glia 61, 1518-1532 (2013).
19. Barros, C. S., Franco, S. J.& Mü ller, U. Extracellular matrix: functions in the nervoussystem. Cold Spring Harb. Perspect. Biol. 3, a005108 (2011).
20. Tissir, F. & Goffinet, A. M. Reelin and brain development. Nature Rev. Neurosci. 4,496-505 (2003).
21. Dufour, A. et al. Area specificity and topography of thalamocortical projections arecontrolled by ephrin/Eph genes. Neuron 39, 453-465 (2003).
22. Gu, C. et al. Neuropilin-1 conveys semaphorin and VEGF signaling during neuraland cardiovascular development. Dev. Cell 5, 45-57 (2003).
23. Cohen, S. et al. A semaphorin code defines subpopulations of spinal motorneurons during mouse development. Eur. J. Neurosci. 21, 1767-1776 (2005).
24. Taniguchi, M. et al. Disruption of semaphorin III/Dgene causes severe abnormalityin peripheral nerve projection. Neuron 19, 519-530 (1997).
25. Zhuo, L. et al. hGFAP-cre transgenic mice for manipulation of glial and neuronalfunction in vivo. Genesis 31, 85-94 (2001).
26. McCall, M. A. et al. Targeted deletion in astrocyte intermediate filament (Gfap)alters neuronal physiology. Proc. Natl Acad. Sci. USA 93, 6361-6366 (1996).
27. Nishiyama, M. et al. Semaphorin 3A induces CaV2.3 channel- dependentconversion of axons to dendrites. Nature Cell Biol. 13, 676-685 (2011).
28. Shelly, M. et al. Semaphorin3A regulates neuronal polarization by suppressingaxon formation and promoting dendrite growth. Neuron 71, 433-446 (2011).
29. Duflocq, A., Chareyre, F., Giovannini, M., Couraud, F. & Davenne, M.Characterization of the axon initial segment (AIS) of motor neurons andidentification of a para-AIS and a juxtapara-AIS, organized by protein 4.1B. BMCBiol. 9, 66 (2011).
30. Arber, S. et al. Requirement for the homeobox gene Hb9 in the consolidation ofmotor neuron identity. Neuron 23, 659-674 (1999).
31. Huber, A. B. et al. Distinct roles for secreted semaphorin signaling in spinal motoraxon guidance. Neuron 48, 949-964 (2005).
32. Camu, W. & Henderson, C. E. Purification of embryonic rat motoneurons bypanning on a monoclonal antibody to the low-affinity NGF receptor. J. Neurosci.Methods 44, 59-70 (1992).
33. Ashrafi, S. et al. Wnt7A identifies embryonic c-motor neurons and reveals earlypostnatal dependence of c-motor neurons on a muscle spindle-derived signal.J. Neurosci. 32, 8725-8731 (2012).
34. Brumovsky, P., Watanabe, M. & Hö kfelt, T. Expression of the vesicular glutamatetransporters-1 and-2 in adult mouse dorsal root ganglia and spinal cord and theirregulation by nerve injury. Neuroscience 147, 469-490 (2007).
35. Brumovsky, P. R. VGLUTs in peripheral neurons and the spinal cord: time for areview. ISRN Neurology 2013, 829753 (2013).
36. Alvarez, F. J., Villalba, R. M., Zerda, R. & Schneider, S. P. Vesicular glutamatetransporters in the spinal cord, with special reference to sensory primary afferentsynapses. J. Comp. Neurol. 472, 257-280 (2004).
37. Mitra, P. & Brownstone, R. M. An in vitro spinal cord slice preparation for recordingfrom lumbar motoneurons of the adult mouse. J. Neurophysiol. 107, 728-741(2012).
38. Behar, O., Golden, J. A., Mashimo, H., Schoen, F. J. & Fishman, M. C. Semaphorin IIIis needed for normal patterning and growth of nerves, bones and heart. Nature383, 525-528 (1996).
39. Averill, S., McMahon, S. B., Clary, D. O., Reichardt, L. F. & Priestley, J. V.Immunocytochemical localization of trkA receptors in chemically identifiedsubgroups of adult rat sensory neurons. Eur. J. Neurosci. 7, 1484-1494 (1995).
40. Ozaki, S.& Snider, W. D. Initial trajectories of sensory axons toward laminar targetsin the developing mouse spinal cord. J. Comp. Neurol. 380, 215-229 (1997).
41. Liu, Y.&Ma, Q.Generation of somatic sensory neuron diversity and implications onsensory coding. Curr. Opin. Neurobiol. 21, 52-60 (2011).
42. Freeman, M. R. & Rowitch, D. H. Evolving concepts of gliogenesis: a look way backand ahead to the next 25 years. Neuron 80, 613-623 (2013).
43. Nagai, M. et al. Astrocytes expressing ALS-linked mutated SOD1 release factorsselectively toxic to motor neurons. Nature Neurosci. 10, 615-622 (2007).
44. Chen, A. I., de Nooij, J. C. & Jessell, T. M. Graded activity of transcription factorRunx3 specifies the laminar termination pattern of sensory axons in thedeveloping spinal cord. Neuron 49, 395-408 (2006).