Development, Vol 121, Issue 5 1341-1350, Copyright © 1995 by Company of Biologists

JOURNAL ARTICLES

Muscle sensory neurons require neurotrophin-3 from peripheral tissues during the period of normal cell death

RA Oakley, AS Garner, TH Large and E Frank
Department of Neurobiology, University of Pittsburgh, School of Medicine, PA 15261, USA.

To determine if muscle sensory neurons require neurotrophin-3 (NT3) during the period of normal cell death, we used an NT3-specific antiserum to deplete NT3 from peripheral tissues during this period in chick embryos. DiI staining of dorsal roots indicated that limb injections of anti-NT3 reduced the spinal projection of muscle spindle afferents. In contrast, injection of the antiserum into the spinal cord had no demonstrable effect, indicating that the reduced projection following limb injection was due to peripheral blockade of NT3 signaling. Counts of neurons retrogradely labeled from muscle and cutaneous nerves showed that peripheral blockade of NT3 selectively reduced the survival of muscle sensory neurons without affecting the survival of cutaneous sensory neurons or motoneurons. In situ hybridization with trkC probes indicated that, during the period of cell death, most large diameter muscle sensory neurons express trkC transcripts, whereas few cutaneous neurons express this receptor for NT3. We conclude that large diameter muscle afferents, including spindle afferents, require NT3 from peripheral tissues to survive the normal period of sensory neuron death in vivo.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				M. Leu, E. Bellmunt, M. Schwander, I. Farinas, H. R. Brenner, and U. Muller Erbb2 regulates neuromuscular synapse formation and is essential for muscle spindle development Development, June 1, 2003; 130(11): 2291 - 2301. [Abstract] [Full Text] [PDF]

				K. Agerman, J. Hjerling-Leffler, M. P. Blanchard, E. Scarfone, B. Canlon, C. Nosrat, and P. Ernfors BDNF gene replacement reveals multiple mechanisms for establishing neurotrophin specificity during sensory nervous system development Development, April 15, 2003; 130(8): 1479 - 1491. [Abstract] [Full Text] [PDF]

				C. Bechade, C. Mallecourt, F. Sedel, S. Vyas, and A. Triller Motoneuron-Derived Neurotrophin-3 Is a Survival Factor for PAX2-Expressing Spinal Interneurons J. Neurosci., October 15, 2002; 22(20): 8779 - 8784. [Abstract] [Full Text] [PDF]

				H.-H. Chen, W. G. Tourtellotte, and E. Frank Muscle Spindle-Derived Neurotrophin 3 Regulates Synaptic Connectivity between Muscle Sensory and Motor Neurons J. Neurosci., May 1, 2002; 22(9): 3512 - 3519. [Abstract] [Full Text] [PDF]

				C. G. Acosta, A. R. Fabrega, D. H. Masco, and H. S. Lopez A Sensory Neuron Subpopulation with Unique Sequential Survival Dependence on Nerve Growth Factor and Basic Fibroblast Growth Factor during Development J. Neurosci., November 15, 2001; 21(22): 8873 - 8885. [Abstract] [Full Text] [PDF]

				V. Coppola, J. Kucera, M. E. Palko, J. Martinez-De Velasco, W. E. Lyons, B. Fritzsch, and L. Tessarollo Dissection of NT3 functions in vivo by gene replacement strategy Development, November 1, 2001; 128(21): 4315 - 4327. [Abstract] [Full Text] [PDF]

				L. M Mendell, J. B Munson, and V. L Arvanian Neurotrophins and synaptic plasticity in the mammalian spinal cord J. Physiol., May 15, 2001; 533(1): 91 - 97. [Abstract] [Full Text] [PDF]

				J. C. Glover Development of Specific Connectivity Between Premotor Neurons and Motoneurons in the Brain Stem and Spinal Cord Physiol Rev, April 1, 2000; 80(2): 615 - 647. [Abstract] [Full Text] [PDF]

				P. Naveilhan, C. Baudet, A. Mikaels, L. Shen, H. Westphal, and P. Ernfors Expression and regulation of GFRalpha 3, a glial cell line-derived neurotrophic factor family receptor PNAS, February 3, 1998; 95(3): 1295 - 1300. [Abstract] [Full Text] [PDF]

				W. M. ElShamy and P. Ernfors Brain-Derived Neurotrophic Factor, Neurotrophin-3, and Neurotrophin-4 Complement and Cooperate with Each Other Sequentially during Visceral Neuron Development J. Neurosci., November 15, 1997; 17(22): 8667 - 8675. [Abstract] [Full Text] [PDF]

				R. H. Friedel, H. Schnurch, J. Stubbusch, and Y.-A. Barde Identification of genes differentially expressed by nerve growth factor- and neurotrophin-3-dependent sensory neurons PNAS, November 11, 1997; 94(23): 12670 - 12675. [Abstract] [Full Text] [PDF]

				G.D. Sterne, G.R. Coulton, R.A. Brown, C.J. Green, and G. Terenghi Neurotrophin-3-enhanced Nerve Regeneration Selectively Improves Recovery of Muscle Fibers Expressing Myosin Heavy Chains 2b J. Cell Biol., November 3, 1997; 139(3): 709 - 715. [Abstract] [Full Text] [PDF]

				R. A. Oakley, F. B. Lefcort, D. O. Clary, L. F. Reichardt, D. Prevette, R. W. Oppenheim, and E. Frank Neurotrophin-3 Promotes the Differentiation of Muscle Spindle Afferents in the Absence of Peripheral Targets J. Neurosci., June 1, 1997; 17(11): 4262 - 4274. [Abstract] [Full Text] [PDF]

				T Ringstedt, J Kucera, U Lendahl, P Ernfors, and C. Ibanez Limb proprioceptive deficits without neuronal loss in transgenic mice overexpressing neurotrophin-3 in the developing nervous system Development, January 7, 1997; 124(13): 2603 - 2613. [Abstract] [PDF]

				I. Shepherd, Y Luo, F Lefcort, L. Reichardt, and J. Raper A sensory axon repellent secreted from ventral spinal cord explants is neutralized by antibodies raised against collapsin-1 Development, January 4, 1997; 124(7): 1377 - 1385. [Abstract] [PDF]

				F. A. White, I. Silos-Santiago, D. C. Molliver, M. Nishimura, H. Phillips, M. Barbacid, and W. D. Snider Synchronous Onset of NGF and TrkA Survival Dependence in Developing Dorsal Root Ganglia J. Neurosci., August 1, 1996; 16(15): 4662 - 4672. [Abstract] [Full Text] [PDF]

				F. Lefcort, D. O. Clary, A. C. Rusoff, and L. F. Reichardt Inhibition of the NT-3 Receptor TrkC, Early in Chick Embryogenesis, Results in Severe Reductions in Multiple Neuronal Subpopulations in the Dorsal Root Ganglia J. Neurosci., June 1, 1996; 16(11): 3704 - 3713. [Abstract] [Full Text] [PDF]

				W. elshamy and P Ernfors Requirement of neurotrophin-3 for the survival of proliferating trigeminal ganglion progenitor cells Development, January 8, 1996; 122(8): 2405 - 2414. [Abstract] [PDF]

				M Ockel, G. Lewin, and Y. Barde In vivo effects of neurotrophin-3 during sensory neurogenesis Development, January 1, 1996; 122(1): 301 - 307. [Abstract] [PDF]