Development, Vol 122, Issue 8 2367-2374, Copyright © 1996 by Company of Biologists

JOURNAL ARTICLES

Late emigrating neural crest cells migrate specifically to the exit points of cranial branchiomotor nerves

C Niederlander and A Lumsden
Department of Developmental Neurobiology, UMDS Guy's Hospital, London, UK.

Morphological segmentation of the avian hindbrain into rhombomeres is also reflected by the emergent organisation of branchiomotor nerves. In each case, the motor neurons of these nerves lie in two adjacent rhombomeres (e.g. of the Vth nerve in r2 and r3, VIIth in r4 and r5 etc.), and their outgrowing axons emerge into the periphery through defined exit points in rhombomeres r2, r4 and r6, respectively. Sensory axons of the cranial ganglia also enter the neuroepithelium at the same points. Motor axon outgrowth through experimentally rotated rhombomeres has suggested that a chemoattractive mechanism, involving the exit points, may form a component of their guidance. Yet so far, nothing is known about the establishment of the exit points or the identity of the cells that form them. In this study, we describe a group of late emigrating cranial neural crest cells which populate specifically the prospective exit points. Using chimaeras in which premigratory chick neural crest had been replaced orthotopically by quail cells, a population of neural crest was found to leave the cranial neural tube from about stage 10+ onwards and to migrate directly to the prospective exit points. These cells define the exit points by stage 12+, long before either motor or sensory axons have grown through them. The entire neural crest population of exit point cells expresses the recently described cell adhesion molecule c-cad7. Further, heterotopic grafting experiments show that midbrain and spinal cord crest, grafted at late stages in place of r4 crest, share the same migratory behaviour to the facial nerve exit points and express the same markers as cells contributed by the native r4 crest. It was not possible to generate new exit points in odd numbered rhombomeres simply by experimentally increasing their (normally insignificant) amount of crest production. Initiation of the exit point region probably lies, therefore, in the neuroepithelium.

This article has been cited by other articles:

				S. Kuratani Is the vertebrate head segmented?--evolutionary and developmental considerations Integr. Comp. Biol., April 17, 2008; (2008) icn015v1. [Abstract] [Full Text] [PDF]

				K. A. Palaisa and M. Granato Analysis of zebrafish sidetracked mutants reveals a novel role for Plexin A3 in intraspinal motor axon guidance Development, September 15, 2007; 134(18): 3251 - 3257. [Abstract] [Full Text] [PDF]

				A. K. Dillon, S. C. Fujita, M. P. Matise, A. A. Jarjour, T. E. Kennedy, H. Kollmus, H.-H. Arnold, J. A. Weiner, J. R. Sanes, and Z. Kaprielian Molecular Control of Spinal Accessory Motor Neuron/Axon Development in the Mouse Spinal Cord J. Neurosci., November 2, 2005; 25(44): 10119 - 10130. [Abstract] [Full Text] [PDF]

				J. Hjerling-Leffler, F. Marmigere, M. Heglind, A. Cederberg, M. Koltzenburg, S. Enerback, and P. Ernfors The boundary cap: a source of neural crest stem cells that generate multiple sensory neuron subtypes Development, June 1, 2005; 132(11): 2623 - 2632. [Abstract] [Full Text] [PDF]

				B. R. Arenkiel, P. Tvrdik, G. O. Gaufo, and M. R. Capecchi Hoxb1 functions in both motoneurons and in tissues of the periphery to establish and maintain the proper neuronal circuitry Genes & Dev., July 1, 2004; 18(13): 1539 - 1552. [Abstract] [Full Text] [PDF]

				J. P. Golding, M. Dixon, and M. Gassmann Cues from neuroepithelium and surface ectoderm maintain neural crest-free regions within cranial mesenchyme of the developing chick Development, January 3, 2002; 129(5): 1095 - 1105. [Abstract] [Full Text] [PDF]

				J. Ghislain, C. Desmarquet-Trin-Dinh, M. Jaegle, D. Meijer, P. Charnay, and M. Frain Characterisation of cis-acting sequences reveals a biphasic, axon-dependent regulation of Krox20 during Schwann cell development Development, January 1, 2002; 129(1): 155 - 166. [Abstract] [Full Text] [PDF]

				A Caton, A Hacker, A Naeem, J Livet, F Maina, F Bladt, R Klein, C Birchmeier, and S Guthrie The branchial arches and HGF are growth-promoting and chemoattractant for cranial motor axons Development, January 4, 2000; 127(8): 1751 - 1766. [Abstract] [PDF]

				D Arendt and K Nubler-Jung Comparison of early nerve cord development in insects and vertebrates Development, January 6, 1999; 126(11): 2309 - 2325. [Abstract] [PDF]

				F Helmbacher, C Pujades, C Desmarquet, M Frain, F. Rijli, P Chambon, and P Charnay Hoxa1 and Krox-20 synergize to control the development of rhombomere 3 Development, January 12, 1998; 125(23): 4739 - 4748. [Abstract] [PDF]

				A Gavalas, M Studer, A Lumsden, F. Rijli, R Krumlauf, and P Chambon Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch Development, January 3, 1998; 125(6): 1123 - 1136. [Abstract] [PDF]

				A Gavalas, M Davenne, A Lumsden, P Chambon, and F. Rijli Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning Development, January 10, 1997; 124(19): 3693 - 3702. [Abstract] [PDF]

				C. Baker, M Bronner-Fraser, N. Le Douarin, and M. Teillet Early- and late-migrating cranial neural crest cell populations have equivalent developmental potential in vivo Development, January 8, 1997; 124(16): 3077 - 3087. [Abstract] [PDF]

				J. Saldivar, J. Sechrist, C. Krull, S Ruffins, and M Bronner-Fraser Dorsal hindbrain ablation results in rerouting of neural crest migration and changes in gene expression, but normal hyoid development Development, January 7, 1997; 124(14): 2729 - 2739. [Abstract] [PDF]

				R Nittenberg, K Patel, Y Joshi, R Krumlauf, D. Wilkinson, P. Brickell, C Tickle, and J. Clarke Cell movements, neuronal organisation and gene expression in hindbrains lacking morphological boundaries Development, January 6, 1997; 124(12): 2297 - 2306. [Abstract] [PDF]