Ectoderm removal prevents cutaneous nerve formation and perturbs sensory axon growth in the chick hindlimb

Developmental Biology

Volumn 266, Issue 1, 2004, Pages 27-42

  Honig, Marcia G ^a   Camilli, Suzanne J ^a   Xue, Qing Shan ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Axon guidance; Chick hindlimb; Cutaneous nerves; Development; Limb innervation; Pathfinding; Sensory axons; Skin innervation; Target cues

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL MATURATION; CHICKEN; CONTROLLED STUDY; ECTODERM; HINDLIMB; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; SKIN; SKIN NERVE;

EID: 0347722286     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2003.10.025     Document Type: Article

References (40)

1. Akita K. The effect of the ectoderm on the dorsoventral pattern of epidermis, muscles and joints in the developing chick leg: a new model. Anat. Embryol. 193:1996;377-386.
2. Amthor H., Christ B., Weil M., Patel K. The importance of timing differentiation during limb muscle development. Curr. Biol. 8:1998;642-652.
3. Araujo M., Piedra M.E., Herrera M.T., Ros M.A., Nieto M.A. The expression and regulation of chick EphA7 suggests roles in limb patterning and innervation. Development. 125:1998;4195-4204.
4. Banerjee S.A., Tessier-Lavigne M., Landmesser L.T. Axon pathfinding in the hindlimb of HGF/SF null mice. Neurosci. Abstr. 24:1998;789.
5. Cahoon S.M., Scott S.A. Multiple mechanisms contribute to the avoidance of avian epidermis by sensory axons. Dev. Biol. 208:1999;502.q-512.q.
6. Cahoon-Metzger S.M., Scott S.A., Wang G. Contribution of BDNF-mediated inhibition in patterning avian skin innervation. Dev. Biol. 232:2001;246-254.
7. Caldero J., Prevette D., Mei X., Oakley R.A., Li L., Milligan C., Houenou L., Burek M., Oppenheim R.W. Peripheral target regulation of the development and survival of spinal sensory and motor neurons in the chick embryo. J. Neurosci. 18:1998;356-370.
8. Donaldson D.J., Mahan J.T. Epidermal cell migration on laminin-coated substrates: comparison with other extracellular matrix and non-matrix proteins. Cell Tissue Res. 235:1984;221-224.
9. Ebens A., Brose K., Leonardo E.D., Hanson M.G. Jr., Bladt F., Birchmeier C., Barres B.A., Tessier-Lavigne M. Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron. 17:1996;1157-1172.
10. Eisen J.S., Pike S.H. The spt-1 mutation alters segmental arrangement and axonal development of identified neurons in the spinal cord of the embryonic zebrafish. Neuron. 6:1991;767-776.
11. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. J. Morphol. 88:1951;49-92.
12. Honig M.G. The development of sensory projection patterns in embryonic chick hindlimb. J. Physiol. (Lond.). 330:1982;175-202.
13. Honig M.G., Kueter J. The expression of cell adhesion molecules on the growth cones of chick cutaneous and muscle sensory neurons. Dev. Biol. 167:1995;563-583.
14. Honig M.G., Rutishauser U.S. Changes in the segmental pattern of sensory neuron projections in the chick hindlimb under conditions of altered cell adhesion molecule function. Dev. Biol. 175:1996;325-337.
15. Honig M.G., Zou J.Y. The effects of target tissues on the outgrowth of chick cutaneous and muscle sensory neurons. Dev. Biol. 167:1995;549-562.
16. Honig M.G., Frase P.A., Camilli S.J. The spatial relationships among cutaneous, muscle sensory, and motoneuron axons during development of the chick hindlimb. Development. 125:1998;995-1004.
17. Honig M.G., Camilli S.J., Xue Q.S. Effects of L1 blockade on sensory axon outgrowth and pathfinding in the chick hindlimb. Dev. Biol. 243:2002;137-154.
18. Lance-Jones C., Landmesser L.T. Pathway selection by chick lumbosacral motoneurones during normal development. Proc. R. Soc. Lond. 214:1981;1-18.
19. Landmesser L.T., Honig M.G. Altered sensory projections in the chick hindlimb following the early removal of motoneurons. Dev. Biol. 118:1986;511-531.
20. Lumsden A.G., Davies A.M. Earliest sensory nerve fibres are guided to peripheral targets by attractants other than nerve growth factor. Nature. 306:1983;786-788.
21. Lumsden A.G., Davies A.M. Chemotropic effect of specific target epithelium in the developing mammalian nervous system. Nature. 323:1986;538-539.
22. Martin P., Khan A., Lewis J. Cutaneous nerves of the embryonic chick wing do not develop in regions denuded of ectoderm. Development. 106:1989;335-346.
23. Niswander L. Interplay between the molecular signals that control vertebrate limb development. Int. J. Dev. Biol. 46:2002;877-881.
24. Oakley R.A., Lefcort F.B., Clary D.O., Reichardt L.F., Prevette D., Oppenheim R.W., Frank E. Neurotrophin-3 promotes the differentiation of muscle spindle afferents in the absence of peripheral targets. J. Neurosci. 17:1997;4262-4274.
25. Patel T.D., Jackman A., Rice F.L., Kucera J., Snider W.D. Development of sensory neurons in the absence of NGF/TrkA signaling in vivo. Neuron. 25:2001;345-357.
26. Phelan K.A., Hollyday M. Axon guidance in muscleless chick wings: the role of muscle cells in motoneuronal pathway selection and muscle nerve formation. J. Neurosci. 10:1990;2699-2716.
27. Riddle R.D., Ensini M., Nelson C., Tsuchida T., Jessell T.M., Tabin C. Induction of the LIM homeobox gene Lmx1 by Wnt7a establishes dorsoventral pattern in the vertebrate limb. Cell. 83:1995;631-640.
28. Saxod R. Development of sensory receptors in birds. Jacobson M. Handbook of Sensory Physiology. vol. 9:1978;338-417 Springer-Verlag, Berlin.
29. Tosney K.W. Proximal tissues and patterned neurite ougrowth at the lumbosacral level of the chick embryo: deletion of the dermamyotome. Dev. Biol. 122:1987;540-588.
30. Tosney K.W., Landmesser L.T. Development of the major pathways for neurite outgrowth in the chick hindlimb. Dev. Biol. 109:1985;193-214.
31. Tosney K.W., Landmesser L.T. Growth cone morphology and trajectory in the lumbosacral regions of the chick embryo. J. Neurosci. 5:1985;2345-2358.
32. Tucker K.L., Meyer M., Barde Y.-A. Neurotrophins are required for nerve growth during development. Nat. Neurosci. 4:2001;29-37.
33. Verna J.M. In vitro analysis of interactions between sensory neurons and skin: evidence for selective innervation of dermis and epidermis. J. Embryol. Exp. Morphol. 86:1985;53-70.
34. Verna J.M., Usson Y., Saxod R. Differential growth of sensory neurons in vitro in presence of dermis and epidermis: a quantitative time-lapse analysis. Cell Differ. 18:1986;183-188.
35. Vogel A., Rodriguez C., Warnken W., Izpisua-Belmonte J.C. Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Nature. 378:1995;716-720.
36. Wang G., Scott S.A. The "waiting period" of sensory and motor axons in early chick hindlimb: its role in axon pathfinding and neuronal maturation. J. Neurosci. 20:2000;5358-5366.
37. Xue Y., Honig M.G. Ultrastructural observations on the expression of axonin-1: implications for the fasciculation of sensory axons during axon outgrowth into the chick hindlimb. J. Comp. Neurol. 408:1999;299-317.
38. Yang Y., Niswander L. Interaction between the signaling molecules WNT7a and SHH during vertebrate limb development: dorsal signals regulate anteroposterior patterning. Cell. 80:1995;939-947.
39. Yip J.W. Target cues are not required for the guidance of sympathetic preganglionic axons. Brain Res. 429:1987;155-159.
40. Zeller J., Schneider V., Malayaman S., Higashijima S., Okamoto H., Gui J., Lin S., Granato M. Migration of zebrafish spinal motor nerves into the periphery requires multiple myotome-derived cues. Dev. Biol. 252:2002;241-256.